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. Author manuscript; available in PMC: 2024 Nov 25.
Published in final edited form as: Acta Trop. 2024 Jan 5;251:107115. doi: 10.1016/j.actatropica.2023.107115

Aedes albopictus is present in the lowlands of southern Zambia

Daniel R Matute *, Brandon S Cooper †
PMCID: PMC11586621  NIHMSID: NIHMS2034535  PMID: 38184292

Abstract

Identifying the current geographic range of disease vectors is a critical first step towards determining effective mechanisms for controlling and potentially eradicating them. This is particularly true given that historical vector ranges may expand due to changing climates and human activity. The Aedes subgenus Stegomyia contains over 100 species, and among them, Ae. aegypti and Ae. albopictus mosquitoes represent the largest concern for public health, spreading dengue, chikungunya, and Zika viruses. While Ae. aegypti has been observed in the country of Zambia for decades, Ae. albopictus has not. In 2015 we sampled four urban and two rural areas in Zambia for Aedes species. Using DNA barcoding, we confirmed the presence of immature and adult Ae. albopictus at two rural sites: Siavonga and Livingstone. These genotypes seem most closely related to specimens previously collected in Mozambique based on CO1 sequence from mtDNA. We resampled Siavonga and Livingstone sites in 2019, again observing immature and adult Ae. albopictus at both sites. Relative Ae. albopictus frequencies were similar between sites, with the exception of immature life stages, which were higher in Siavonga than in Livingstone in 2019. While Ae. albopictus frequencies did not vary through time in Livingstone, both immature and adult frequencies increased through time in Siavonga. This report serves to document the presence of Ae. albopictus in Zambia, which will contribute to the process of determining the potential public health implications of this disease vector in Central Africa.

INTRODUCTION

Diseases transmitted by Dipteran vectors represent one of the most important threats facing public health (Gubler 2009; Schmidt et al. 2013; Danasekaran et al. 2014; Torto and Tchouassi 2021). Approximately half of the world population may be at risk of contracting a vector-borne disease over their lifetime (Danasekaran et al. 2014; Torto and Tchouassi 2021), many of which are life-threatening and cause enormous cost to the patients and local public health systems they affect. The disease burden of Dengue, for example, seems to be largely unreported (Bhatt et al. 2013) and yet has risen dramatically over the last three decades (Bhatt et al. 2013; Du et al. 2021; Tian et al. 2022). Vectors are also important because they are effective conduits of zoonotic diseases that are a significant threat to human populations (Karesh et al. 2012; Schmidt et al. 2013; Gibb et al. 2020). The impact of vectors on public health is likely to increase as changing climates and anthropogenic activities influence species’ ranges and their contacts with human populations (Carlson et al. 2023; Longbottom et al. 2023).

Mosquitoes from the genus Aedes pose a significant threat to human health on multiple continents. Aedes aegypti is the primary vector of viral diseases such as dengue and yellow fever. Each year at least 50,000 patients die because of dengue (Wilder-Smith et al. 2010), and at least 30,000 because of yellow fever (Barnett 2007). These numbers are likely underestimated (Rigau-Pérez 2006; Barnett 2007; Allwinn et al. 2008; Adalja et al. 2012; Beaumier et al. 2014). Aedes aegypti is endemic to West Africa and has spread to more than 120 countries distributed across the globe (Rose et al. 2023). It has been hypothesized that Ae. aegypti range expansion has occurred for at least the last 500 years (Christophers 1960; Lounibos 2002)—this expansion may be as fast as 250 km per year in North America (Kraemer et al. 2019). A second species, Ae. albopictus, is endemic to Southeast Asia and has spread to all continents in the last five decades (Hawley 1988; BENEDICT et al. 2007; Paupy et al. 2009). In places like North America and Europe, the Ae. albopictus may be spreading over 100 km per year (Kraemer et al. 2019). Both species are expected to expand their geographic ranges as global temperatures increase (Fischer et al. 2014; Kamal et al. 2018; Kraemer et al. 2019; Liu et al. 2019; Laporta et al. 2023). This expansion is likely to impact human populations that have typically not been impacted by primarily tropical diseases.

In areas where vector-borne diseases are endemic, the invasion of Ae. albopictus is of particular importance for public health. Even though Ae. albopictus has historically been considered a secondary vector of dengue and yellow fever (reviewed in (Paupy et al. 2009)), recent work has demonstrated that Ae. albopictus is a competent vector of both diseases (Gloria-Soria et al. 2020). Ae. albopictus is also a vector of Zika and Chikungunya (Vega-Rúa et al. 2014; Garcia-Luna et al. 2018; McKenzie et al. 2019; Gloria-Soria et al. 2020), two emergent viral diseases with notable disease burden (Puntasecca et al. 2021). For example, in Cameroon and Gabón, the presence of Ae. albopictus was associated with epidemics of these two diseases in 2007 (Grard 2014). Both Ae. aegypti and Ae. albopictus are also potential vectors of other arboviruses that include Japanese encephalitis virus (Rosen et al. 1985), West Nile virus (Zhang et al. 2022), eastern equine encephalitis virus (Scott et al. 1990; Mitchell et al. 1992; Turell et al. 1994), and La Cross Virus (Gerhardt et al. 2001; Jackson et al. 2014; Westby et al. 2015). Thus, understanding the geographic distribution of these vectors remains critical.

Aedes albopictus is now prevalent across remote areas of Central Africa (Djiappi-Tchamen et al. 2021; Montgomery et al. 2022; Canelas et al. 2023; Obame-Nkoghe et al. 2023). The expansion, thus, has the potential to induce strain in health systems that are already overburdened. However, it is possible that Ae. albopictus might outcompete Ae. aegypti, through competitive exclusion ((O’meara et al. 1995; Britch et al. 2008; Juliano 2010) but see (Chan et al. 1971; Parker et al. 2019)), or satyrization (Zhou et al. 2022), which ultimately might reduce the population sizes of the more effective vector, Ae. aegypti. Understanding the precise geographic range of Ae. albopictus is an important public health issue that can answer the relative importance of the species as a disease vector and as a competitor in the vector species community, but one that can only be addressed with meticulous field collections.

Zambia is one of the few countries on the African continent where Ae. albopictus has not been formally observed (Gubler 2003; Longbottom et al. 2023). Based on its wider distribution in Africa, we hypothesized that Ae. albopictus is likely present in Zambia. To test this, we sampled the Aedes of seven locations in Zambia in 2015, and two strategically chosen sites in 2019. We discovered both immature and adult Ae. albopictus individuals at two sites in southern Zambia and in both years, with Ae. albopictus frequency increasing through time in one. Based on this temporal and spatial presence of Ae. albopictus, we suggest that Ae. albopictus is a resident species in the lowlands of Zambia. We report that Ae. albopictus may be generally increasing in frequency, but this increase is unlikely to be rapid enough to displace Ae. aegypti in the near future. The isolates we observe are most closely related to isolates from Mozambique based on mtDNA barcoding. Our results will likely contribute to local control strategies, as the two species show differences in their preferred habitats.

METHODS

Locations

We sampled Aedes in seven different locations in 2015. This included sampling the boundaries of four major Zambian cities: Lusaka, Livingstone, Chipata, and Mazabuka. We also sampled three rural areas, including near Luangwa National Park, Siavonga (on the shores of Lake Kariba), and Shesheke. The 2019 sampling was strategically restricted to only two of these sites based on our 2015 observations: Livingstone and Siavonga. Table 1 lists the coordinates of the collection sites and the number of days that we sampled them.

TABLE 1.

Coordinates and sampling outcomes of the 2015 and 2019 sampling sites.

2015 2019
Altitude (m) Coordinates Days Imm. Adults Days Imm.
Lusaka (C) 1,274.9 −15.504919, 28.265470 4 0 0 NA NA NA
North Luangwa national park (O) 595.1 −12.060373, 32.356497 5 0 0 NA NA NA
Chipata (C) 1,184.7 −13.621321, 32.652523 5 0 0 NA NA NA
Mazabuka (C) 1,045.6 −15.861312, 27.712943 3 0 0 NA NA NA
Sesheke (O) 952.3 −17.484532, 24.331769 5 0 0 NA NA NA
Siavonga (O) 509.2 m −16.542560, 28.689792 5 1 2 5 15 14
Livingstone (C) 903.7 m −17.871160, 25.857488 5 1 5 5 3 7
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NA indicates that the site was not sampled in 2019. Imm: Immatures.

Insect collections

Our goal was to determine the presence and frequency of immature and adult Ae. albopictus at the sites we sampled. To sample immatures, we collected larvae and pupae (collectively referred to as immature stages) by placing 32oz Ziploc containers (Reference number: 70937) with fish food and water, outside buildings (ovitraps). We then waited for an average of 3 to 5 days (Table 1), checking daily to make sure that animals did not disturb the traps. Immature stages were collected for ten days using a plastic pipette and placed in individual borosilicate vials. Each specimen was then inspected for taxonomically informative traits (See below).

To collect adults, we used CDC-type light traps (2836BQX, BioQuip; Rancho Domingo, CA) connected to a 6V as a power source. We used a mixture of yeast and water as a source of CO2. The trap was operated for three days at a time, but the collection sack was removed and the 6V battery was replaced every 48 hours. All the insects collected in the trap were removed from the traps using a mouth aspirator (1135A Aspirator–BioQuip; Rancho Domingo, CA), and anesthetized with FlyNap (Carolina Biological Supply Company, Burlington, NC). The totality of the collection was placed in a Petri dish and inspected under a Leica dissecting scope.

Species identification

We differentiated between Ae. albopictus and Ae. aegypti larvae using a non-destructive procedure and two diagnostic traits. In Ae. aegypti, the comb scale on the terminal segment has a single row of pitchfork-shaped scales; larvae also have strong black hooks in the side of the thorax. In Ae. albopictus, the comb scale in the terminal segment is also in one row, but the scales are thorn-shaped and the hooks on the side of the thorax are small or absent (Lee 1998). Pupae were differentiated by the shape and length of the terminal setae in the paddle. While Ae. aegypti has short and simple terminal setae at the edge of the paddle, Ae. albopictus has long hairs (Penn 1949). Larvae and pupae were kept in glass vials until they hatched and were inspected for adult traits that differentiate them. In Ae. albopictus the scutum has one silvery-white stripe down its middle, the thorax has patches of silver scales and a black clipeus. In Ae. aegypti, the scutum has a lyre-shaped pattern of white scales, a clipeus with white scales. Our field designations were then confirmed using genetic data.

MtDNA typing

To confirm the accuracy of our field identifications using morphological traits, we used a mtDNA marker, cytochrome oxidase I (COI) to type species. Previous studies have shown that COI-based DNA barcoding is able to differentiate between species of Aedes, and other mosquito genera (Chan et al. 2014). We extracted DNA from single mosquitoes using the Qiagen DNeasy Blood and Tissue Kit (Qiagen Inc., Valencia, CA). We then amplified ~25 ng of total DNA using PCR and conditions previously reported (Chan et al. 2014), using the two following primers: 5’-AAAAAGATGTATTTAAATTTCGGTCTG-3’ and 5’-TGTAATTGTTACTGCTCATGCTTTT-3’. Briefly, the amplification cycles were as follows: 94°C for 1 min followed by (34 cycles at 94°C for 30 seconds, annealing temperature: 52°C for 30 seconds, 72°C for 1 min 30 seconds), and a single final step at 72°C for 7 min. All amplifications were performed using a 2720 Thermal Cycler from Applied Biosystems (Foster City, CA).

PCR products were sent for sequencing to Eton Biosciences (NC) using the same PCR primers. Sequencing of PCR fragments was performed using the cyclic reaction termination method (Sanger sequencing) using the BigDye Terminator Cycle Sequencing Kits (Applied Biosystems, Foster City, CA, USA). To minimize false polymorphism, we sequenced both DNA strands, aligned them, and examined them with 4Peaks 1.7.1 (http://nucleobytes.com/index.php/4peaks). We extracted DNA from 31 adult individuals, and successfully PCR-amplified 24 samples (all samples collected in 2023) and obtained COI sequences from 18 amplicons. The resulting two haplotypes (See Results and Discussion) were deposited in Genbank (Accession numbers: TBD).

We obtained previously published sequences of Ae. albopictus to infer a crude genealogy of the species (Table S1), and to determine the most closely related geographic samples to our collections from Zambia. We used this COI alignment to generate a maximum-likelihood phylogenetic tree with IQTREE (Nguyen et al. 2015; Minh et al. 2020), using automatic inference of the model of molecular evolution (option -m), and a random seed (752482). We rooted the tree using Ae. aegypti (voucher ZOOMENTAa8, genBank accession number: MK265729). We used ultrafast bootstrap to calculate the branch support of each node (Minh et al. 2013; Hoang et al. 2018)

RESULTS AND DISCUSSION

Our sampling revealed the presence of Ae. albopictus in two out of the seven locations that we sampled in Zambia: Siavonga (509m) and Livingstone (903m). Environmental niche models have previously predicted Siavonga as a favorable site for Aedes occurrence (Velu et al. 2021). Aedes albopictus was absent from collections we made at the three urban locations with higher altitude (Lusaka: 1,275; Mazabuka: 1,046m; and Chipata: 1,185m) and from two of the other rural locations (North Luangwa National Park: 595m, and Shesheke: 952m).

Next, we studied the frequency of Ae. albopictus relative to Ae. aegypti in Siavonga and Livingstone. In 2015, the relative proportion of immature Ae. albopictus individuals was similar in Siavonga (1.5%) and Livingstone (2%; χ2 < 0.01, df = 1, P = 1). The relative proportion of Ae. albopictus adults also did not differ significantly between sites (Siavonga = 3.1%, Livingstone = 8.3%, χ2 = 0.788, df = 1, P = 0.375). In 2019, immature stages of Ae. albopictus were proportionally more abundant in Siavonga (14%) than in Livingstone (3%, χ2 = 8.03, df = 1, P = 4.6 × 10−3), but again there was no significant difference in the relative frequency of Ae. albopictus adults between the two locations (Siavonga: 18.4%, Livingstone: 8%, χ2 = 3.119, df = 1, P = 0.077). These results motivate a large-scale and longitudinal study of Ae. albopictus abundance in the lowlands of Zambia.

We also studied whether the relative proportion of Ae. albopictus varied between years in Siavonga and Livingstone. Between 2015 and 2019, the proportion of Ae. albopictus immature individuals increased from 1.5% to 14% in Siavonga (χ2 = 6.713, df = 1, P = 9.573 × 10−3) but the relative proportion of Ae. albopictus immature individuals did not not change between years in Livingstone (2–3%; χ2 < 0.01, df = 1, P = 0.95). We observed a similar result for adults, where adult Ae. albopictus became more common in Siavonga, increasing in frequency from 3.1% to 18.4% between 2015 and 2019 (χ2 = 6.745, df = 1, P = 9.40 × 10−3); but the relative proportion of Ae. albopictus adults remained similar between years in Livingstone (8.3%–8.0, χ2 < 0.01, df = 1, P= 1).

The absence of Ae. albopictus from locations with an elevation over 1,000 meters is also noteworthy. While several environmental niche modeling efforts have suggested that Ae. albopictus may have the capacity to expand its range into higher altitudes (Fischer et al. 2014; Echeverry-Cárdenas et al. 2021; Santos et al. 2022), longitudinal sampling of mountainous regions in Zambia and other areas of Africa is needed to test this hypothesis. Sampling of other continents supports Ae. albopictus expansion into higher altitudes. For example, Ae. albopictus occurs at significantly higher altitudes in South America than the median altitude in Zambia (~1,200m). In Colombia, Ae. albopictus is routinely sampled at altitudes similar to Lusaka in Zambia (up to 1,300m, (Echeverry-Cárdenas et al. 2021)). In a more extreme case, Ae. albopictus was recently sampled in Bolivia at an elevation of over 2,300m (Ríos et al. 2023). Together, these observations suggest that while altitude may influence rates of Ae. albopictus’ dispersal, it is not an insurmountable barrier for its establishment.

We next used COI sequence from mtDNA to infer the general genetic relationships among the specimens of Ae. albopictus we sampled from Zambia and isolates collected in other countries. Zambia is a landlocked country, but it shares borders with countries in the Indian Ocean. This proximity is relevant because the first observations of Ae. albopictus in Africa were from samples collected from Indian Ocean islands (Madagascar: 1904, Mauritius: 1922, Seychelles: 1977, reviewed in (Longbottom et al. 2023)). We find that the isolates of Ae. albopictus we sampled from Siavonga, Zambia are closely related to other mtDNA haplotypes present in Mozambique, suggesting that the invasion in Zambia likely occurred via migration from adjacent countries. Notably, we observe two different COI Ae. albopictus haplotypes, both of which are present in Mozambique. Of the 18 individuals that we typed using COI sequence, 12 have a COI haplotype identical to a sample collected in Mozambique (LC726293.1), and six have a haplotype identical to a second Mozambique specimen (LC726392.1). While DNA barcoding is powerful for species identification, the typing here is inherently limited for the identification of demographic events. The inference of the events and population of origin that lead to the presence of Ae. albopictus in Zambia will require more systematic insect sampling and sequencing of whole genomes.

While we do not currently know the full distribution of Ae. albopictus in Zambia, or across Africa more broadly, our observation of Ae. albopictus at two sites in two years significantly contribute to current knowledge by establishing that by 2015 Ae. albopictus colonized the southern lowlands of Zambia (under 1,000 m above the sea level); and in the case of Siavonga, our results indicate that the relative frequency of Ae. albopictus is increasing through time. Notably, surrounding counties such as Mozambique (Kampango and Abílio 2016; Abílio et al. 2018), Tanzania (Patrick et al. 2017), and the Democratic Republic of the Congo (Bobanga et al. 2018; Vulu et al. 2021) had reported the presence of Ae. albopictus at a similar time (2015–2016). This may indicate recent expansion of Ae. albopictus into these countries and Zambia. In contrast, it is plausible that Ae. albopictus has gone undetected, and successful independent sampling of each country randomly occurred at a similar time.

The finding of Ae. albopictus in Zambia is of importance for public health because several diseases transmitted by Aedes species—including Dengue, yellow fever, and Chikunguya—are present in Zambia. For example, a serological survey revealed that 4.1% of participants from Western and North-Western Zambia were seropositive for Dengue (N = 3,624, (Mazaba-Liwewe et al. 2014)). In central Zambia, the proportion of Dengue seropositive patients seems to be higher (16.8%, N = 214; (Chisenga et al. 2020)). The same survey found that 36.9% of patients from Central Zambia were seropositive for Chikungunya, 10.8% for Zika, and 19.6% for Mayaro (Chisenga et al. 2020). To our knowledge, no serological prevalence surveys for any of these diseases exist for areas where we have sampled Ae. albopictus. However, there is evidence that Zika exists in this region, with twenty samples out of 50 from non-human primate samples (Chlorocebus cynosuros and Papio ursinus, (Wastika et al. 2019)) having anti-Zika antibodies. This suggests that non-human primates might serve as Zika virus reservoirs in areas where we sampled Ae. albopictus. Other diseases are also worth considering. For example, West Nile virus has also been isolated from other mosquitoes (Orba et al. 2018), humans (Mweene-Ndumba et al. 2015) and potential reservoir species (Simulundu et al. 2020); and Ae. albopictus is an effective vector of West Nile virus (Zhang et al. 2022). The confluence of these vectors and pathogens they may plausibly transmit motivates future analyses focused on better understanding disease prevalence across Zambia and other regions of Africa.

Supplementary Material

Table S1, FIgure S1

FIGURE 1. Sites included in this study.

FIGURE 1.

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We collected seven different sites, four of which were at the boundaries of urban centers (C) and three of which were in rural areas. Two sites, Siavonga and Livingstone (marked with a star) were sampled in 2015 and 2019.

FIGURE 2. Maximum likelihood tree derived from the COI mtDNA barcode.

FIGURE 2.

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We retained all the branches in spite of some low-support branches. Values above each node correspond to the bootstrap support. Depicted branch lengths are not proportional to facilitate the interpretation of the genealogical relationships. Figure S1 shows a scaled tree.

ACKNOWLEDGEMENTS

We would like to thank the Matute lab for helpful comments. DRM was supported by the National Institute of General Medical Sciences under Award R35GM148244. BSC was supported by the National Institute of General Medical Sciences under Award R35GM124701.

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Table S1, FIgure S1
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