Synanthropic Culicidae in three fragments of Atlantic Forest in northern Paraná, BrazilABSTRACT
Culicidae are implicated in arboviruses and represent a public health concern. The objective of this study was to understand the diversity and population dynamics of synanthropic Culicidae sheltered in forest fragments, pointing out potential vectors of agents etiological. Culicidae were sampled using traps in three forest fragments (Daher Wood, Botanical Garden, and Mata dos Godoy State Park) in Londrina, Paraná, Brazil. To sample Culicidae, six traps were deployed along two parallel 70-m transects, spaced 30 m apart. Each transect contained three oviposition traps, comprising bamboo internode traps and tire traps in equal numbers. Five genera and eight species were collected, totaling 15,048 specimens. The peri-urban fragments showed the highest richness. Tires were preferred as breeding sites. The seasons of the highest and lowest sampling were summer (6 species and 7,295 specimens) and winter (4 species and 696 specimens). The Daher Wood and Botanical Garden showed high similarity, and the Godoy Wood, an intact environment, showed the greatest dominance. Mosquitoes showed different synanthropy levels (Culex saltanensis = + 97 and Toxorhynchites theobaldi = - 0.4). Correlations were positive between temperature (r = 0.53) and precipitation (r = 0.40) with Culicid abundance. The Principal Component Analysis indicated that tires were most influenced by temperature, relative humidity, and bamboo by total dissolved solids. Four collected species showed vector potential. High diversity occurred in warmer and rainy periods. Vector species in these areas are of concern because they may alter arbovirus cycles, making continuous monitoring essential.
Keywords:
Abiotic variables; Traps; Population dynamics; Synanthropic; vector species
Introduction
The Atlantic Forest biome is one of the regions with the greatest biodiversity of fauna and flora on the planet. Initially, it covered approximately 1.3 million km2 along the entire Brazilian coast, encompassing 17 states. However, only 24% of the native vegetation remains; of this, only 12.4% comprise mature, well-preserved forests, and most of the remaining area is fragmented and disconnected. Considering only well-preserved forest remnants larger than half a hectare, only 12.4% remain (Rezende et al., 2018; Safar et al., 2020, SOSMA, 2024).
The intense reduction in the original vegetation cover and the consequent environmental fragmentation may favor populations of species with greater adaptability and resistance to environmental changes. Among them, several species of mosquitoes belonging to the Culicidae family (Diptera) stand out, such as the native species Haemagogus (Conopostegus) leucocelaenus Dyar, 1925 and exotic species Culex (Culex) quinquefasciatus Say 1823, Aedes (Stegomyia) aegypti Linnaeus, 1762, and Aedes (Stegomyia) albopictus Skuse, 1894 (Zequi et al., 2005; Fimia et al., 2022). Urban forest fragments affected by human activity tend to contain not only wild species, but also opportunistic exotic species and vectors of etiological agents. This occurs because mosquitoes have rapid reproduction, genetic and ecological plasticity, and can migrate to the urban environment where they find conditions that favor their development, mainly due to the availability of natural and artificial breeding sites used by females for oviposition, becoming abundant in areas that previously had low species richness (Lopes, 1997; Taipe-Lagos and Natal, 2003; Leisnham et al., 2004; Zequi et al., 2005; Chaves et al., 2011; Zahouli et al., 2017; Montagner et al., 2017; Fimia et al., 2022; Nascimento et al., 2022).
Various characteristics of breeding sites influence the choice of oviposition site, such as color, consistency, size, and shape (Nunes-Silva et al., 2020). In altered landscapes, the distribution and availability of breeding sites change, favoring synanthropic species (Montagner et al., 2017; Almeida et al., 2020).
Changes in the behavior of vector mosquitoes may have epidemiological implications, facilitating the emergence or reappearance of arboviroses (Bellini et al., 2022). Alterations in population dynamics caused by human actions often benefit these vector species, affecting nearby human populations and those engaged in surrounding activities (Guedes and Navarro-Silva, 2014). Given the above, it is essential to understand how these environmental changes influence the distribution and diversity of culicids.
Therefore, the objective of this study was to investigate the occurrence of synanthropic Culicidae species in an urban area, a peri-urban area, and a preserved forest fragment of the Brazilian Atlantic Forest. Furthermore, the study aimed to evaluate the diversity of Culicidae in these environments, their degree of synanthropy, observing the seasonal population fluctuation of the group and distinguishing vector species of etiological agents for monitoring and control purposes.
Material and methods
Study area
The study area is in the municipality of Londrina, northern Paraná, Brazil, with geographical coordinates of -23.14639° and -23.92944° south latitude and -50.87306° and -51.31972° west longitude. The municipality has a territorial area of 1,652.569 km2, with a climate characterized as warm subtropical, with long, muggy summers and short winters. Throughout the year, the average temperature varies between 13°C and 30°C, with precipitation throughout the year (Weatherspark, 2023).
Sampling was carried out between July 2016 and May 2017, in three forest fragments of the Brazilian Atlantic Forest located in the municipality of Londrina: Bosque Daher (MD) (–23.315278 S and –51.204444 O), Botanical Garden (BG) (–23.362222 S and –51.172778 O), and a preserved fragment in the Mata dos Godoy State Park (MG) (–23.448056 S and –51.255833 O). Bosque Daher is an urban forest reserve covering an area of 3.3 hectares, located in the urban area of Londrina. The Botanical Garden is a peri-urban area with over 100 hectares of native forest, with the presence of exotic species, springs and rivers. The Mata dos Godoy State Park has 790 hectares of Semideciduous Seasonal Forest, made up of flat areas, where the Ribeirão dos Apertados is located, and slopes, reaching an altitude of 470 m.
Collection and identification of synanthropic mosquitoes
In each fragment, two 60 m transects were drawn in parallel, with 30 meters between them. Each transect contained three traps. For car tires were used – 13-inch rims, cut transversely. Bamboo internodes (Bambusa sp.) measuring 25 cm high and 12.5 cm wide were used as internode traps. In each transect, the traps were positioned 10 m from the edge of the fragment, with a spacing of 30 m between them, all at ground level. After positioning, distilled water was added to the traps (tire: 1.5 L; bamboo: 1 L) (Figure 1), and the volume was replenished weekly during the collection period. The physicochemical parameters of the water (pH, temperature, conductivity, salinity, dissolved and saturated oxygen, and TDS) in the breeding sites were sampled using a HannaⓇ multiparameter model HI9828. Temperature and relative humidity were monitored continuously using a thermo-hygrometer that was installed in the fragments between the transects. Rainfall data was provided by the Agronomic Institute of Paraná (IAPAR) (23°22'S and 51°10'W).
Schematic representation of data collection carried out in three forest fragments of the Brazilian Atlantic Forest located in the Northern Region of Paraná, Brazil between 2016 and 2017. (The figure is schematic and not to scale). Map elaborated using QGIS software.
Biotic and abiotic data were sampled quarterly, with five consecutive weekly collections per fragment. To capture the immature Culicidae, the water from the breeding sites was strained through a sieve (1 mm mesh; 12 cm diameter) and then added to plastic bottles with ventilated lids (7.5 cm diameter and 400 mL). The material collected was sent to the Medical Entomology Laboratory at the State University of Londrina and after sorting, the specimens were deposited in the Entomological Collection of the State University of Londrina.
Immature specimens that were not identified through their larval morphology were reared to the adult stage or to the fourth larval instar for later identification with the aid of an Olympus CH30 LF100 stereo optical microscope. The fourth instar larvae were mounted on semi-permanent slides with Hoyer's fluid. The dichotomous keys of Consoli and Oliveira (1994) and Forattini (2002). The species identified were confirmed with specimens from the Padre Jesus Santiago Moure Entomological Collection at the Federal University of Paraná.
Statistical analysis
To calculate the degree of synanthropy of Culicidae, the index of Nuorteva (1963) was used with modifications. The index follows the formula: IS = 2a + b – 2c/2, where: a = percentage of a species x sampled in the urban area in relation to the same species sampled in the rural area and in the forest; b = percentage of species x in the rural area; c = percentage of species x in the forest. In this study, the areas were altered, being a = fragment in the interior of the municipality (Daher; urban area); b = fragment located in the peri-urban area and rural (Jardim Botânico); c = fragment with forest (Godoy). This index ranges from +100 to -100, with positive values indicating a high degree of synanthropy and negative values indicating the opposite.
To measure diversity, the Shannon-Wiener (H') and Margalef (Dmg) indices were used; for species dominance, the Simpson (C) and Berger-Parker (d) indices were used; and to verify equitability the Shannon-Wiener (eH') and Pielou (J) indices were chosen, performed using the DiVes Program – Species Diversity 3.0 (Rodrigues, 2014). The similarity between the fragments was calculated using the Morisita and Bray-Curtis Index, performed in Past 3.0 Software (Hammer, 1999). To test differences in the richness and abundance of mosquitoes between fragments and between types of breeding sites, the T-test, ANOVA, and Kruskal-Wallis tests were used with Fisher's post-hoc for the former and Dunn's test for the latter in Statistica Software (StatSoft, 2005).
Regarding sampling, species rarefaction curves were created for the fragments and species richness was estimated with the help of the non-parametric Jackknife (I and II) and Chao (I and II) extrapolator indices (estimators). The data used to assemble the curves and calculate estimators were obtained through a randomization process in the Estimate-S 9.1.0 program (Colwell, 2016). Temperature, relative humidity, and precipitation data were correlated with insect abundance using linear correlation in Statistica software (Statsoft 7.0). To verify the abiotic parameters, namely temperature, relative humidity, precipitation, pH, conductivity, salinity, total dissolved solids (TDS), saturated dissolved oxygen, and their influence on the oviposition sites analyzed, Principal Component Analysis (PCA) was used through Past 3.0 software (Hammer, 1999).
Results
During the sampling period 15,048 Culicidae specimens were collected and distributed in five genera and eight species. The peri-urban fragment (BG) had the highest richness, with eight species, followed by the urban fragment (MD), with seven species, and finally the preserved environment (MG), with five species. The most abundant species were Culex (Culex) eduardoi Casal and Garcia 1968 (9,326 specimens) and Limatus durhamii Theobald 1901 (4,832 specimens) and the least abundant were Culex (Culex) saltanensis Dyar, 1928 (17 specimens) and Ae. (Stg.) aegypti (7 specimens). The species Cx. (Cux.) eduardoi was less abundant in the peri-urban fragment and in the preserved area. The species Cx. (Cux.) saltanensis, Ae. (Stg.) aegypti and Ae. (Stg.) albopictus were not sampled in the preserved fragments (Table 1).
Total abundance, Nortueva Index, and classification (native or exotic) of Culicidae species collected in forest fragments of the Brazilian Atlantic Forest between July 2016 and May 2017 in the Northern region of Paraná, Brazil. MD: Mata Daher; BG: Botanical Garden; MG: Mata dos Godoy; AT: Total or absolute abundance; I.N: Nortueva Index (1963); Cl: Classification as to whether it is native (N) or exotic (E).
The degree of the synantropy varied among the studied species. Culex (Cux.) saltanensis, Ae. (Stg.) aegypti and Ae. (Stg.) albopictus showed a stronger affinity for the forested areas impacted by human activities, exhibiting the highest synantropy values. Conversely, Hg. (Con.) leucocelaenus, Aedes (Protomacleaya) terrens, and Cx. (Cux.) eduardoi preferred preserver environments. Toxorhynchites (Lynchiella) theobaldi Dyar and Knab, 1906 and Li. durhamii, in turn, exhibited a uniform distribution across the study areas (Table 1).
Artificial traps were characterized as the preferred breeding ground for mosquitoes, with a colonization rate of 90.55% and a share of 88% of the larvae sampled, compared to natural breeding grounds, which had a colonization rate of 38.89% and a share of 12% of the larvae found. In addition, artificial breeding sites were also more productive when considering population density and species diversity, as seven species were found mainly in artificial breeding sites.
About the richness and abundance of mosquitoes among the fragments and among the types of breeding sites, it was identified that there was a significant difference only between the Botanical Garden and the Mata dos Godoy (p = 0.015). Types of breeding sites in total were also significantly different (p < 0.001), as were types of breeding sites per area, with (p < 0.001) in Daher, (p < 0.001) in the Botanical Garden and (p < 0.001) without Godoy. Regarding the type of breeding ground related to the three areas, the bamboos among the three areas showed important differences between Daher and Godoy (p = 0.010) and between Botanical Garden and Godoy (p= 0.006), while the tires did not show significant differences between the areas. As for species richness, there were no significant differences in any of the cases compared (Table 2).
Diversity, Dominance, and Evenness Indices of Culicidae collected in three forest fragments of the Brazilian Atlantic Forest between July 2016 and May 2017, in the Northern region of Paraná, Brazil.
The genus Aedes Meigen 1818 was represented by three species. Aedes (Stegomyia.) aegypti few representatives were only sampled in the fall in the urban and peri-urban fragments. The Ae. (Stg.) albopictus was more abundant during spring and summer in the urban and peri-urban fragments, showing no specific preference for breeding site. The Ae. (Pro.) terrens were sampled in both breeding sites and in all fragments, with a peak in abundance in summer and no representatives collected in winter.
The Morisita index showed similar values between 0.976 and 0.992 for urban and peri-urban fragments, and the Bray-Curts index values between 0.84 and 0.9. The peri-urban fragment showed a higher species richness, according to the Margalef index (2.018). However, Pielou's evenness index indicated a uniformity of individuals of 0.464, a value lower than that observed in the urban fragment (0.521), revealing that despite the high richness, the distribution of individuals among the species in the peri-urban environment was less diverse compared to the other fragments (Table 2).
Sampling during all climatic seasons made it possible to discover a greater number of species, as they have preferences for certain periods, influenced by environmental characteristics and the biology of each species. Regarding mosquito abundance, statistical analyses showed a moderate correlation of 0.530 with temperature and a correlation of 0.400 with precipitation, with p < 0.050. Relative air humidity did not show a significant correlation. Figure 2 presents the abundance of Culicidae in relation to abiotic factors.
Abundance of Culicidae collected between July 2016 and May 2017 in three forest fragments of the Brazilian Atlantic Forest and their relationship with temperature, relative air humidity, and precipitation in the Northern region of Paraná, Brazil.
Principal component analysis (PCA) revealed that the tires and the bamboo internodes are close together, suggesting that the area is not influencing the choice of breeding site (Figure 3). The bamboo breeding site was more influenced by relative humidity and precipitation (external to the breeding site) when compared to other variables (internal to the breeding sites). On the other hand, the bamboo breeding site did not show such an explicit approximation of the abiotic variables, being only slightly closer to the TDS variable when compared to the other variables. The low richness obtained by the Chao I, Chao II, Jackknife I and Jackknife II estimators shows that, despite estimating a few more species for the fragments, this number was not significant. Figure 4 shows the species rarefaction curves for the three fragments, where the sampling sufficiency can be seen.
Principal Component Analysis resulting from the ordering of breeding sites according to abiotic variables.
Rarefaction curves of Culicidae species sampled in the three fragments of Brazilian Atlantic Forest evaluated in the period between July 2016 and May 2017.
Discussion
In fragmented habitats, species richness declines due to the extinction or migration of wild species (Anjos and Navarro-Silva, 2008). However, some Culicidae species can adapt to new selective pressures in this altered environment (Chaves et al., 2011). The greater richness in urban and peri-urban fragments revealed that the species sampled prefer altered locations. In these environments, there is strong anthropic action, with the disposal of garbage, tires, and other containers, which increase the number of artificial breeding sites and end up becoming refuges for species of mosquitoes with a synanthropic nature (Zequi et al., 2005). More preserved areas tend to have a greater richness of wild Culicidae species (Anjos and Navarro-Silva, 2008).
The preference for artificial breeding sites is linked to the genetic plasticity and synanthropic biology of species in their search for oviposition sites. They benefit from environmental changes caused by humans and take advantage of containers with stored water for oviposition (Zequi et al., 2005).
The genus Aedes was represented by three species, Ae. (Stg.) aegypti, Ae. (Stg.) albopictus, and Ae. (Pro.) terrens. Of these, the first two are exotic and the last is native to Brazil, and all carry pathogens. The species Ae. (Stg.) aegypti is associated with humans and is highly dependent on manufactured containers for oviposition. The presence of Ae. (Stg.) aegypti in the peri-urban fragment reveals some situations: the presence of disposable garbage and other containers that are used for the reproduction of this species, which helps to maintain the population in these forest fragments, but forest fragments and nearby populations maintain a population of Ae. (Stg.) albopictus (Montagner et al., 2017). Despite the low number of representatives sampled, Ae. (Stg.) aegypti has been associated with Ae. (Stg.) albopictus. These are species that, despite having different niches, are distributed in the same habitats (Leandro, 2012) and develop in the same types of artificial containers. The decrease in Ae. (Stg.) aegypti is related to an increase in Ae. (Stg.) albopictus because in places where they co-occur, Ae. (Stg.) albopictus was shown to be a superior competitor (Leisnham et al., 2014). The ecological valence of Ae. (Stg.) albopictus causes it to have a wide occupation, colonizing wild and anthropic environments, and natural and artificial breeding sites (Forattini, 2002; Zequi et al., 2005).
Aedes (Protomacleaya) terrens is a species with more sylvatic habits, however it can be found in anthropized environments (Zequi et al., 2005). It was collected in the three areas, but with most individuals in the Mata dos Godoy and with a preference for oviposition in tires. It was known to reproduce only in natural breeding sites such as tree holes (Neves and Faria, 1977); however, it began to be recorded in artificial breeding sites from 1988 onwards (Zequi et al., 2005). Despite the low number of representatives sampled (7) always associated cohabiting with Ae. (Stg.) aegypti and Ae. (Stg.) albopictus. However, it is frequently found cohabiting with most species that use tires as breeding sites (Lopes, 1997). Its greatest abundance occurred in the summer, characterized by high temperature and precipitation, corroborating Zequi et al. (2005) who recorded high average populations in the hot and rainy months.
In the present study, the presence of Hg. (Con.) leucocelaenus was identified in artificial breeding sites in the peri-urban study area. It exhibits diurnal, acrodendrophilic habits, with records of searching for hosts found at ground level (Vasconcelos, 2003; Pinto et al., 2009; Gomes et al., 2010), however, it has also been recorded in residences inhabited by humans (Camargo-Neves et al., 2005; Gomes et al., 2010; Cardoso et al., 2010), demonstrating its capacity for domiciliation, an alarming situation given that the aforementioned species is responsible for the transmission of the sylvatic yellow fever virus. According to the Ministry of Health, from January to April 2025, 110 cases and 44 deaths from yellow fever were recorded. In all cases, exposure to wild and/or forested areas was reported, whether due to occupational or recreational activities.
The occurrence of Cx. (Cux.) saltanensis, represented almost entirely in winter, showed a preference for lower temperatures and little rain, diverging from Cx. (Cux.) eduardoi. This species was shown to be adapted to milder temperatures, which are more suitable for its development and provide lower fertility losses and lower mortality rates in adult mosquitoes. The totality of individuals inhabiting artificial breeding sites and the majority being found in the urban environment reveal the high adaptability of this species to modified environments, in accordance with the synanthropic index. Despite this, this species can also be found colonizing natural breeding sites (Zequi and Lopes, 2012).
Culex (Culex) eduardoi and Li. durhamii were the dominant species, colonizing both types of breeding sites, during all seasons in all fragments. This abundance was also verified in other studies (Zequi et al., 2005; Montagner et al., 2017). Both species were found in the three fragments, because they have euryoecious characteristics and present genetic plasticity that makes them able to survive in anthropic environments and colonize natural and artificial breeding sites.
Limatus durhamii could colonize different environments and breeding sites due to its high ecological valence, and its development can occur in natural and artificial breeding sites (Silva et al., 2004), being, in general, the first species to establish itself (Lopes et al., 1987),
Culex (Cux.) eduardoi also has a wide ecological valence and for this reason it is found in natural and anthropic environments, colonizing natural breeding sites and artificial breeding sites, with a preference for tires (Lopes, 1997). However, despite preferring artificial breeding sites for oviposition, these species inhabit the different areas studied and for this reason their degrees of synanthropy were relatively low. These results may be linked to the strong association of Li. durhamii with native forests (Montagner et al., 2017), while Cx. (Cux.) eduardoi prefers breeding sites in shaded areas and closed forests (Lopes et al., 2012) demonstrating sensitivity to environmental degradation.
The abundance of Culicidae populations is closely associated with abiotic factors, mainly temperature, precipitation, and relative humidity, which directly influence the seasonal activity of mosquitoes and their interaction with the pathogen-host (Costa et al., 2010; Roiz et al., 2014; Bellone and Failloux, 2020). Temperature can affect the development (Ludwig et al., 2019), survival (Buxton, 1933; Reeves et al., 1994), geographic dispersal (Ng et al., 2019; Koloski et al., 2021), and vector competence of mosquitoes (Paz, 2015). Rainfall influences the availability and maintenance of breeding sites (Wijesundera, 1988; Rakotoarinia et al., 2022), determining the viability of immature stages through the accumulation of water in natural or artificial breeding sites (Clements, 1992). Relative air humidity can impact mating, dispersal, longevity, hematophagy, and oviposition, affecting the population dynamics of mosquitoes (Day, 2016; Holmes and Benoit, 2019). Given the above, culicid populations tend to decrease as Culicidae species are reduced in the coldest periods and increased in the hottest and rainiest periods. This is because the temperature directly influences their development, and an increase of 1º C can cause a 54% increase in the female's egg laying (Nascimento et al., 2022). Consistent with the correlations (PCA and linear correlation), a greater abundance of mosquitoes is generally associated with higher temperatures, humidity and high precipitation rates.
Some relationships between the larvae of different species in the breeding sites were verified. In most traps, Tx. (Lyn.) theobaldi was present with Li. durhamii and/or Cx. (Cux.) eduardoi but was also found cohabiting with the other species. Aedes (Stegomyia) aegypti larvae were always found sharing breeding sites with Ae. (Stg.) albopictus, and Ae. (Pro.) terrens cohabiting with Hg. (Con.) leucocelaenus. However, Ae. (Stg.) albopictus and Ae. (Pro.) terrens did not frequently live on the same breeding site. The greatest cohabitation was in the summer, all of them occurring in the preserved fragments and always presenting the same species, namely, Cx. (Cux.) eduardoi, Li. durhamii, Ae. (Pro.) terrens, Hg. (Con.) leucocelaenus, and Tx. (Lyn.) theobaldi. Due to the great abundance in the warmer seasons, the search for oviposition sites by females is greater, which is why artificial breeding sites can generally house a wide diversity of species (Zequi et al., 2005).
Conclusion
Abiotic factors such as temperature, humidity, and precipitation directly influence mosquito biology, resulting in greater abundance during warm and rainy periods. Variation in the degree of synanthropy revealed that some species show a greater preference for disturbed areas, which should be frequently evaluated, since wild mosquitoes may exhibit phenotypic plasticity and dynamic occupancy of these spaces.
The presence of several species with the potential to transmit etiological agents found in these areas highlights the importance of epidemiological surveillance, especially in urban and peri-urban fragments. Studies such as this one provide important information about the species and enable the development of new and effective strategies aimed at the efficient monitoring of Culicidae in anthropogenic areas.
The data indicated the need to monitor these areas due to the presence of vectors of pathogens and wild species in more altered environments. This adaptive capacity to disturbed environments can generate alterations in the epidemiological conditions of infectious agents. Knowledge about this group is far from complete and more information about changes in biology, activity, oviposition behavior, and susceptibility to insecticides contributes to the creation of new strategies to control vector species in these areas close to human populations.
Acknowledgments
We would like to thank researcher Dr. Mário Navarro for his contributions to the project and the Federal University of Paraná for granting access to the Padre Jesus Santiago Entomological Collection.
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Funding
Capes 001 - Luis Eduardo Grossi.
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