Taxonomy, Ecology and Distribution of the Mosquitoes (Diptera: Culicidae) of the Dutch Leeward Islands, with a Key to the Adults and Fourth Instar Larvae

Contributions to Zoology 89 (2020) 373-392 CTOZ brill.com/ctoz

Taxonomy, ecology and distribution of the mosquitoes (Diptera: Culicidae) of the Dutch Leeward Islands, with a key to the adults and fourth instar larvae

Jordy G. van der Beek Naturalis Biodiversity Center, Leiden, the Netherlands [email protected]

Klaas-Douwe B. Dijkstra Naturalis Biodiversity Center, Leiden, the Netherlands

Berry B. van der Hoorn Naturalis Biodiversity Center, Leiden, the Netherlands

Sam P. Boerlijst Institute of Environmental Sciences, Leiden University, Leiden, the Netherlands

Loes Busscher Naturalis Biodiversity Center, Leiden, the Netherlands

Maud L. Kok Naturalis Biodiversity Center, Leiden, the Netherlands

Marieta A.H. Braks Netherlands National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands Francis Schaffner Francis Schaffner Consultancy, Riehen, Switzerland

Gerald J. Davelaar Ministry of Public Health, Social Development and Labour, Sint Maarten, Caribbean Netherlands

Maria Henry Ministry of Public Health, Social Development and Labour, Sint Maarten, Caribbean Netherlands

© van der Beek et al., 2020 | doi:10.1163/18759866-bja10005 This is an open access article distributed under the terms of the cc by 4.0 license. Downloaded from Brill.com09/26/2021 02:03:44AM via free access

374 VAN DER BEEK et al.

Koen Hulshof Netherlands National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands. Public Health Department, Saba, Caribbean Netherlands

Teresa E. Leslie Eastern Caribbean Public Health Foundation, Sint Eustatius, Caribbean Netherlands

Maarten Schrama Naturalis Biodiversity Center, Leiden, the Netherlands Institute of Environmental Sciences, Leiden University, Leiden, the Netherlands

Abstract

Assessing mosquito biodiversity is important for disease surveillance and ecosystem health assessments. Such studies are particularly needed in regions like the Caribbean, which have experienced a series of recent mosquito borne disease outbreaks but received little attention regarding its invertebrate biodiversity. Here, we report on results from a mosquito survey on the Dutch Leeward Islands (Sint Eustatius, Sint Maarten and Saba), carried out in April and October 2018, which is the first integrative survey since those conducted by Van der Kuyp (1947) and Wagenaar Hummelinck (1949). Moreover, we present a novel key for adults and fourth instar larvae of the mosquitoes of the Dutch Leeward Islands. Overall, eleven species were recorded, eight on Sint Maarten, five on Saba and two on Sint Eustatius. Two new potential disease vectors, Culex nigripalpus and Aedes taeniorhynchus, were recorded on Sint Maarten. One previously recorded species, Cx. habilitator, was not retrieved from any of the islands, which is further discussed in the paper. Species indicative of natural forest which previously occurred on all three islands were absent from Sint Eustatius and Sint Maarten but still present on Saba. In contrast, species indicative of human inhabi- tation, Ae. aegypti and Cx. quinquefasciatus, were highly abundant on Sint Maarten and Sint Eustatius and present in low numbers on Saba. Overall, the results of this study emphasize the importance of biodiversity surveys and indicate that frequent mosquito inventories may contribute to a better understanding of mosquito community composition and distribution of potential vector species.

Keywords biodiversity assessment – Culex nigripalpus – mosquito survey – Saba – Sint Eustatius – Sint Maarten

Introduction such as dengue, chikungunya, malaria, Zika, Rift Valley and West Nile fever (Rueda, 2008). Mosquitoes (Diptera: Culicidae) present a ma- As a result of anthropogenic disturbance of jor risk for human health worldwide (WHO, mosquito habitats, urbanization, internation- 2017). Not only are they often a nuisance, but al trade and travel and spread of invasive mos- can also serve as vectors for a wide range of hu- quitoes, the distributions of mosquito species man and livestock pathogens causing diseases have exhibited majorDownloaded changes from Brill.com09/26/2021 over the past 02:03:44AM via free access

MOSQUITOS OF THE DUTCH LEEWARD ISLANDS 375 decades (Lambin et al., 2010; Neiderud, 2015; southeast of Sint Eustatius, recorded two spe- Egizi et al., 2016; Eritja et al., 2017). The possi- cies not recorded from the Dutch Leeward Is- ble forthcoming knock-on effects on the lands: Ae. tortilis and Cx. nigripalpus (Moham- emergence of novel pathogens highlight the med et al., 2015). importance of (more) frequent mosquito bio- Currently, mosquito research on the Dutch diversity surveys. The Caribbean is a promi- Leeward Islands has a strong focus on Ae. ae- nent example of a region that is experienc- gypti, the principle vector for chikungunya, ing high levels of travel, urbanization and dengue and Zika viruses, and to a lesser extent anthropogenic disturbance (Debrot et al., on Cx. quinquefasciatus, a vector of West Nile 2018) and has recently witnessed a series of virus (Couch, 2013; Leslie et al., 2014, 2017; major mosquito-borne disease outbreaks (i.e., Glandorf, 2017). When a mosquito-borne dis- the 2014 chikungunya outbreak, the 2016 Zika ease emerges, suppression of the vector popu- outbreak, several dengue outbreaks) (Matheus lation is in most cases the only way to respond et al., 2012; Henry et al., 2017; Leslie et al., 2017) to the outbreak. However, to be effective, re- and the region is currently witnessing another cent updated information about the distribu- dengue outbreak (PAHO, 2020). The impor- tion of mosquito species as well as the occur- tance of mosquito surveys in the Caribbean rence and habitat use of potential vector is further exemplified by lack of recent spe- species is essential for all three islands. For cies distribution data, in combination with example, populations of Ae. albopictus and the dramatic loss of natural habitats (Debrot Ae. taeniorhynchus are present on other is- et al., 2018) and the global spread of invasive lands in the Caribbean region (Belkin & mosquitoes (Kraemer et al., 2019). Heinemann, 1976; Benedict et al., 2007; Mo- The last mosquito species inventories on hammed et al., 2015), but the current distribu- Sint Eustatius, Sint Maarten and Saba were tion of these potential vector species on the performed in 1947 (Van der Kuyp, 1948, 1949, Dutch Leeward Islands is not well known. 1954) and later by Wagenaar Hummelinck in Moreover, mosquito identification keys for 1949 (Van der Kuyp, 1953, 1954). Based on these islands are outdated or simply not avail- these surveys, Van der Kuyp (1954) listed elev- able. These knowledge gaps complicate ade- en species from the islands: Aedes aegypti, Ae. quate risk assessments and control efforts busckii, Ae. taeniorhynchus, Anopheles albima- of species other than Ae. aegypti and high- nus, Culex americanus [= Cx. bisulcatus], Cx. light the need to acquire information on spe- bahamensis, Cx. habilitator, Cx. quinquefascia- cies’ current distributions and practical mos- tus, Deinocerites magnus, Psorophora pyg- quito identification tools (Farajollahi & Price, maea and Toxorhynchites guadeloupensis. 2013). Other islands in the Caribbean with more The aim of this research was to obtain a comprehensive and recent mosquito surveys better understanding of the current distribu- have listed many more species, including a tion of various mosquito species on the Dutch number of important disease vectors such Leeward Islands. To this end, we carried out as Ae. albopictus (Benedict et al., 2007) and an intensive one-week survey on each of the Cx. nigripalpus (Schaffner, 2003; Mohammed three islands (Sint Eustatius, Sint Maarten et al., 2015). In total over 70 mosquito species and Saba) during the dry season and a total of have been recorded from the Leeward and ten days during the wet season on Sint Windward Islands (excluding Trinidad and Maarten and Saba. We created an easy-to-use Tobago) (Gaffigan et al., 2019). A 2010 survey identification key for both the fourth instar of Saint Kitts, an island located only 10 km larvae and the adultsDownloaded specifically from Brill.com09/26/2021 to the species 02:03:44AM via free access

376 VAN DER BEEK et al. present on these islands based on the collect- larvae using an aquatic net, a turkey baster ed data. and an electric pipet (Integra Biosciences™ Pi- petboy). The type of aquatic habitat from each larval collection site was recorded. Natu- Material and methods ral and semi-natural habitats included bromeliads, Heliconia inflorescences, tree holes, crab Sampling and identification holes, rock and beach pools, permanent The Dutch Leeward Islands comprise three is- ponds, temporary ponds, and ditches. The ar- lands in the northeastern part of Caribbean tificial habitats include man-made containers Sea: Sint Eustatius (17°29’ N, 62°58’ W), Saba (e.g., buckets, car tires), wells, troughs, aban- (17°38’ N, 63°14’ W) and Sint Maarten (18°4’ N, doned swimming pools, and cisterns (fig. 2). 63°3’ W). The island of Sint Maarten consists of A selection of the collected mosquito lar- a Dutch and French part. Saba and Sint Eusta- vae was reared to adult stage using a BioQuip® tius are special municipalities within the King- Mosquito Breeder (BioQuip Products Inc., dom of the Netherlands and Sint Maarten is a USA). A subset of the collected adults of each constituent country within the Kingdom of the species was mounted and kept for future ref- Netherlands. Together, these three islands have erence. The remainder of the collected mos- a surface area of 68 km2. Each of the islands was quito larvae was preserved in 96% ethanol. visited during an expedition by Naturalis Bio- The collection has been stored at the Natu- diversity Center in April 2018 and sampled for ralis Biodiversity Center, formerly the Nation- one week. The French part of the island, Saint al Museum of Natural History, Leiden, the Martin, was not sampled due to the limited Netherlands (RMNH). The mounted adults time and administrative restrictions. Sint are stored under collection number RMNH. Maarten and Saba were revisited in October INS.1114057-4101. The larvae are stored under 2018 for ten days of additional sampling. collection number RMNH.INS.1114151-159 and Ten trapping sites were selected in urban, RMNH.INS.1269669-9719. semi-urban and relatively natural areas (fig. 1). All adult mosquitoes were morphologically Selection of these sites was based on exist- identified by using newly developed keys (in- ing vegetation maps (Verweij, 2010; De Freitas cluded after the Discussion), which were et al., 2012, 2016), knowledge on the presence based on available specimens, species de- of different aquatic habitats and former sam- scriptions, and pre-existing identification pling localities of Van der Kuyp (1954). We keys for the region (such as: Lane, 1953; Van used four different collection methods. First, der Kuyp, 1954; Pratt, 1969; Belkin et al., 1970; at each site, a Mosquito Magnet® Indepen- Darsie et al., 2010; Gustave et al., 2018). All dence (Woodstream Corp., USA) mosquito morphospecies from the sites were DNA bar- trap was used to trap adults. Second, Biogents coded as mini-barcodes for MT-CO1 by using a (BG) Sentinel Traps™ (Biogents AG, Germany), Culicid-specific primer (Boerlijst et al., 2019; with the BG Lure™ and a sugar-and-yeast mix- Krol et al., 2019). Morphological identifica- ture as a CO2 source were used at two to three tions were checked by blasting the barcodes sites per island. Specimens from all traps were against the Barcode of Life Data (BOLD) Sys- collected once every 24 hours for four consec- tem (version 4) and a reference database ex- utive days. Third, at each site, we used a net tracted from a small collection of pinned and aspirator to sample free-flying adults. adults from Guadeloupe provided by one of Finally, aquatic habitats were sampled for the authors (FS) (RMNH.INS.1114107-134). All

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MOSQUITOS OF THE DUTCH LEEWARD ISLANDS 377

Figure 1 Sample sites of mosquitoes on Sint Eustatius, Saba and Dutch Sint Maarten during the 2018 Naturalis expeditions. The sampling methods referred to as “Other” comprise of different manual methods to sample adults and larvae. Sites with a BG-sentinel trap or other sampling method that was within 50 m of a Mosquito Magnet site are not separately shown on this map. Map created with QGIS, basemap. © OpenStreetMap contributors and the GIS user community.

Figure 2 Different habitat types that were sampled during the 2018 survey. Natural habitats: a) Bromelias, b) inflorescences of Heliconia sp. c) rock pool/beach pool, d) crab hole; Semi-natural habitats: e) temporary/permanent pond, Artificial habitats: f) bucket, g) well, h) car tire, i) abandoned swimming pool, j) cistern. Photos courtesy of K.-D.B. Dijkstra, J.G. van der Beek and K. Hulshof.

Downloaded from Brill.com09/26/2021 02:03:44AM via free access 378 VAN DER BEEK et al. extracted reference barcodes are available in Results the “Culicidae Caribbean (MEDLI)” project on BOLD (www.boldsystems.org). A total of 831 adult mosquitoes was trapped To inspect whether the mosquito species and examined during the 2018 survey. The communities differ between the islands and number of larvae was not assessed, because whether the different habitat types contain only a subsample of larvae was collected from different mosquito communities, nonmetric each of the habitats. Eleven species of mos- multidimensional scaling (NMDS) analyses quitoes, belonging to six genera, were record- were conducted in RStudio (version 1.2.5019) ed on all islands combined. Eight species were with R version 3.6.1 (supplementary figs. S1 recorded from Sint Maarten, five from Saba and S2). Results are discussed in the (species and only two from Sint Eustatius (table 1). The specific) sections below. most collected species were Cx. quinquefasciatus (56 % of adults) and Ae. aegypti (35 % of Taxonomic treatment adults). Aedes taeniorhynchus and Cx. nigri- Species names follow the generic and sub- palpus were recorded for the first time for the generic classification of Harbach & Howard island of Sint Maarten. (2007), except for the species from the tribe There were some notable differences in lar- Aedini (in this case all Aedes and Psorophora val habitat use between species (table 2; sup- species). Nomenclature of the latter follows plementary figs. S1 and S2). Six species were Wilkerson et al. (2015), where most genera are observed only in natural and semi-natural returned to sub-generic status. habitats: Cx. bisulcatus; Cx. habilitator, Cx. nigripalpus, De. magnus, Ps. pygmaea and Tx. cf. Construction of morphological guadeloupensis. Some of these species were identification keys observed in a single habitat type only: Cx. bi- To facilitate identification, we constructed a sulcatus only occurred in plant containers, dichotomous, literature-based identification and De. magnus in crab holes. None of the ob- key for the mosquitoes of the Dutch Leeward served species were completely restricted to Islands, which is included after the Discus- artificial habitats, although the occurrence in sion. Aside from the species recorded from semi-natural habitats was rare for the larvae the islands, the invasive mosquito Ae. albopic- of Ae. aegypti and Cx. quinquefasciatus (less tus is included, because it is likely to spread than 9 % of positive sites). across the Caribbean, as well as Ae. tortilis, a species present on the neighboring islands. The key is based on previous keys from the Discussion Caribbean region (Lane, 1953; Van der Kuyp, 1954; Pratt, 1969; Belkin et al., 1970; Darsie et al., Historically, eleven mosquito species were re- 2010; Gustave et al., 2018). Additional charac- corded on the Dutch Leeward Islands. During ters were added from species (re)descrip- the 2018 survey, ten of these were retrieved. In tions, standard reference works and (sub)ge- addition, Ae. taeniorhynchus and Cx. nigripal- neric revisions (Bram, 1967; Berlin, 1969a; pus were recorded for the first time for Sint Berlin & Belkin, 1980). Where possible, the key Maarten. For each of the separate islands the was improved after examination of collection percentage of retrieved species was markedly material from the 2018 survey and material al- lower than in the survey by Van der Kuyp ready present in the collection of Naturalis Bio- (1954). Five (83%) of the previously recorded diversity Center (Leiden, The Netherlands). species were foundDownloaded again on from Saba, Brill.com09/26/2021 six (75%) 02:03:44AM via free access

MOSQUITOS OF THE DUTCH LEEWARD ISLANDS 379

Table 1 Overview of the mosquito species of the Dutch Leeward Islands. This table includes the results of the 2018 Naturalis survey (●) as well as that of Van der Kuyp (1954) (○) Sint Maarten Saba Sint Eustatius Aedes (Howardina) busckii (Coquillett, 1906) ● ○ Aedes (Ochlerotatus) taeniorhynchus (Wiedemann, 1821) ●1 ●2 Aedes (Stegomyia) aegypti (Linnaeus, 1762) ● ● ● Anopheles (Nyssorhynchus) albimanus Wiedemann, 1820 ● Culex (Culex) bahamensis Dyar & Knab, 1906 ● ○ Culex (Culex) habilitator Dyar & Knab, 1906 ○3 Culex (Culex) nigripalpus Theobald, 1901 ●1 Culex (Culex) quinquefasciatus Say, 1823 ● ● ● Culex (Micraedes) bisulcatus (Coquillett, 1906) ○ ● ○ Deinocerites magnus (Theobald, 1901) ● Psorophora (Grabhamia) pygmaea (Theobald, 1903) ● Toxorhynchites (Lynchiella) cf. guadeloupensis (Dyar & Knab, 1906) ● 1New record for Sint Maarten. 2Record by Cornel et al. (2020). 3Doubtful record, see the discussion.

Table 2 Overview of the habitats used by the different mosquito species of the Dutch Leeward Islands, based only on data from the islands of Sint Eustatius, Sint Maarten and Saba. The table includes the results of the 2018 Naturalis survey (●) as well as that of Van der Kuyp (1954) (○) Natural and semi-natural habitats Artificial habitats inflorescences Bromeliads Heliconia holes Tree Crabholes pools Rock Beach pools ponds Permanent ponds and ditches Temporary Artificial containers and cisterns troughs Wells, Ae. aegypti ○ ● ● Ae. busckii ● ○ ● Ae. taeniorhynchus ● ○ An. albimanus ●1 ○ Cx. bisulcatus ● Cx. bahamensis ● ○ ● Cx. habilitator2 ○ Cx. nigripalpus ● ● Cx. quinquefasciatus ● ● ● De. magnus ● Ps. pygmaea ● Tx. cf. guadeloupensis ● ● 1No larvae were found during this survey. This habitat type represents the most prominent larval habitat of this species on neighboring islands. Downloaded from Brill.com09/26/2021 02:03:44AM 2Doubtful record, see the discussion. via free access

380 VAN DER BEEK et al. on Sint Maarten and two (40%) on Sint type locality: Dominica [erroneously stated to Eustatius. The vast majority of adults trapped be San Domingo in original description (fide with the Mosquito Magnet® belonged to Howard et al., 1917)]). Northern adults have a the group of ‘indicators of anthropogenic larger white ring on segment 3 of the hind tar- activity’, which suggests that for surveys on sus, while the larvae have a larger patch of these islands a combination of larval sam- comb scales and pecten teeth that reaches as pling and hand-sampling of adult mosquitoes far as the siphonal hairs (Berlin, 1969b). The at dawn may be more effective than using male genitalia of the northern population dif- traps. fer in having more hairs and a broader ae- Although we visited the island in the same deagus, with distinct lobes at the tip (Berlin, month (April) as Van der Kuyp, we are not 1969b). The Saba population shows probably able to compare mosquito abundances be- northern character states, but this cannot be tween the 1947 and 2018 surveys. Van der confirmed because the diagnostic characters Kuyp did not mention much about his sam- are not quantified in literature and material pling strategy and the number of sampled in- from its southern distribution was not avail- dividuals is lacking for most of the mosquito able for comparison to the authors. Whether species. there is genetic differentiation is not known Below, we discuss habits, occurrences and as barcodes from southern populations are changes therein for each species separately, in unavailable. alphabetic order. Moreover, we discuss the po- Interestingly, Ae. busckii larvae were not tential methodological shortfalls of this study, found in bromeliads on Saba (this study and the overall changes in mosquito communities Richardson & Richardson, 2014) and have for each of the islands, and the overall pat- only rarely been found there on other islands terns of change. (Berlin, 1969b). Whether this is due to differences in water quality, competition with Cx. Remarks on species bisulcatus or predator avoidance (e.g., Tx. gua- Aedes (Howardina) busckii (Coquillett, 1906) deloupensis) is unclear. Aedes busckii was recorded from a tree hole on Sint Eustatius (Van der Kuyp, 1948, 1954) and Aedes (Ochlerotatus) taeniorhynchus recorded as the most abundant mosquito spe- (Wiedemann, 1821) cies (71 %) in water held by Heliconia caribaea This is the first time that Ae. taeniorhynchus is inflorescences on Saba (Bass & Bass, 2011). recorded on Sint Maarten. Adults of this spe- Larvae were found both in Heliconia bracts cies were collected in the Belvedere district and in rainwater on the lid of a rain barrel on near the French border next to an open drain Saba (Bud’s Mountain Trail and Crispeen and a small pond, close to a marsh. Van der Trail, approx. 17°37’50” N, 63°14’30” W). We did Kuyp (1954) reported that this species often not observe Ae. busckii on Sint Eustatius, like- co-occurs with Anopheles species. Interesting- ly as a result of the lack of water in tree holes ly, we trapped Ae. taeniorhynchus in conjuc- and the absence of Heliconia flowers during tion with An. albimanus at this site. Further- our visit. more, larvae were collected at a different site The distribution of Ae. busckii is restricted close to Mullet Bay Golf Course from stagnant to the Lesser Antilles, from Saba to Grenada. rainwater on the course. This location is close Berlin (1969b) noted that the northern popu- to the American University building of the lations (Sint Eustatius to Guadeloupe) differ Caribbean School of Medicine where adults from the southern ones (which includes the were trapped by studentsDownloaded (Colin from Brill.com09/26/2021 Michie, pers. 02:03:44AM via free access

MOSQUITOS OF THE DUTCH LEEWARD ISLANDS 381 comm., 27 July 2018). Van der Kuyp (1953, 1954) on human blood and is therefore mainly also reports Ae. taeniorchynchus from a well at found close to habitation (Harrington et al., Spring Bay, Saba. Despite our best efforts, both 2001). It is the main vector for a number of ar- in April and October we were not able to find boviruses in the Caribbean causing dengue, this species there again. However, during a chikungunya and Zika (Leslie et al., 2014, subsequent study, a female of this species was 2017). As expected, we found Ae. aegypti pres- trapped with a BG-Sentinel Trap in the har- ent in urban habitats on all three islands. We bour of Saba by one of the authors (Cornel also found Ae. aegypti in high densities in two et al., 2020) (Yoosook Lee, pers. comm., 1 Sep- remote old wells on Sint Eustatius (Venus Bay tember 2019), which shows that this species is Road, 17°30’17.8“ N, 62°58’59.4” W; Smoke Al- still occurring on the island. ley [near Fort Rotterdam], 17°29’13.1“ N, Antillean adults of Ae. taeniorhynchus are 62°59’36.0” W). One of these wells had a rela- described to be darker overall than their con- tively high salinity of 7 ‰, which has been tinental conspecifics (Belkin et al., 1970). This shown to be well within the tolerance range of is most pronounced in the reduced white Ae. aegypti (De Brito Arduino et al., 2015). Ver- rings on the hind tarsus, with only a very small donschot and Besse-Lototskaya (2014) con- basal white ring on the 5th segment. Previous- cluded from a meta-analysis of 62 dispersal ly, these dark specimens have been described studies that Ae. aegypti can cover maximally by Giles (1904) and Ludlow (1905) as two sepa- distances of 2.5 km (mean = 333 m). Reiter rate species: Ae. niger and Ae. portoricensis. et al. (1995) reported that furthest Ae. aegypti Howard et al. (1917) noted the absence of dif- post-blood meal flight was 441 m (mean = 181 ferences in the male genitalia and larvae be- m). In a 200 m radius around the wells, only tween both forms, and suggested the dark one or two residences are present, whereas form was a “geographic race” of Ae. goats were extremely abundant on this part of taeniorhynchus. this island. The fact that post-blood meal flights over 200 m are exceptional and densi- Aedes (Ochlerotatus) tortilis (Theobald, 1903) ties of adult mosquitoes at both sites were ex- Aedes tortilis has never been recorded on any ceptionally high suggests that Ae. aegypti at of the Dutch Leeward Islands, but occurs these localities may be partly feeding on non- throughout the Lesser Antilles (Arnell, 1976) human hosts. Other studies have shown that and is present on the neighboring Virgin Is- the percentage of Ae. aegypti that were blood- lands (Dyar, 1922) and Saint Kitts (Moham- fed on humans varies from 76.2 % in rural med et al., 2015). Therefore, it is likely that Puerto Rico (Barrera et al., 2012), where other this species is present, on one of the Dutch is- hosts were mainly dogs, but also on cats, hors- lands and it is therefore included in the adult es, and chickens, to 99.1 % in Thailand (Ponla- and larval identification keys. The larval habi- wat & Harrington, 2005). On Sint Eustatius, tats generally occur in temporary or semi- goats and sheep are very abundant at these permanent fresh to brackish groundwater sites. However, further research is needed to pools (Arnell, 1976), conditions that are omni- examine the origin of the blood meals. present on Sint Maarten. Aedes (Stegomyia) albopictus (Skuse, 1894) Aedes (Stegomyia) aegypti (Linnaeus, 1762) Another invasive mosquito species, Ae. albop- The invasive Ae. aegypti was probably intro- ictus is present on other Caribbean islands duced in the 16th century (Lounibos, 2002). It such as Barbados, Cayman Islands, Cuba, breeds in artificial containers and feeds mainly Dominican RepublicDownloaded and from Trinidad,Brill.com09/26/2021 but 02:03:44AM has via free access

382 VAN DER BEEK et al. not yet been confirmed for the three focal is- also been recorded from fresh water and is oc- lands (Benedict et al., 2007). Due to intensive casionally found in artificial containers on travel and transport to the Dutch Leeward Is- other islands (Belkin et al., 1970). On Sint Eu- lands, establishment seems probable. We statius, this species had previously been re- therefore included this species in both the corded from a well near ‘Oranjebaai’ by Van adult and larval identification keys. At the der Kuyp (1948, 1949, 1954). Despite our effort time of writing there is no definitive evidence to sample from the exact same well (17°29’13.1“ to support the presence of Ae. albopictus on N, 62°59’36.0” W), the species was not found. the Dutch Leeward Islands. Instead, we trapped adults of Ae. aegypti at the well and collected large numbers of larvae Anopheles (Nyssorhynchus) albimanus from the slightly brackish well water. Wiedemann, 1820 Anopheles albimanus had been recorded once Culex (Culex) habilitator Dyar en Knab, 1906 as larvae from a well in Rockland on Sint Although Van der Kuyp (1948, 1949, 1954) re- Maarten by Van der Kuyp (1953, 1954). During ported Cx. habilitator from land crab holes on our survey, adults were caught in Belvedere Sint Maarten (Rolandus Channel and Lower district near the French border, which is ap- Princess Quarter) often together with De. mag- proximately two kilometers from the place nus, we did not find any. The identification of where Van der Kuyp observed this species. this species is problematic as adults look very Van der Kuyp (1954) mentioned the finding similar to Cx. bahamensis, whereas the lar- of An. “tarsimaculatus” [sic] on French Saint vae resemble Cx. nigripalpus. Despite the fact Martin by B.J. Emanuels in the 1920s. At the that Van der Kuyp collected both larvae and time, the name tarsimaculatus was invalidly adults, and therefore identification should proposed as emendation for An. albipes by be easy, his description of the larvae does not Goeldi (1905). Both names are now recognized agree with diagnostic characters described by as synonyms of An. albimanus (fide Roze- Bram (1967). The larvae of Van der Kuyp have boom & Gabaldon, 1941). We assume Emanu- “anal gills, about as long as the segment, with els’ finding of An. albimanus to be correct be- blunt tips” and are pictured with a double api- cause there are no other Anopheles species cal tuft on the siphon; the gills should be short, present on the neighboring islands, and Faran pointed, and the tuft should be triple. This sug- (1980) also recorded this species from French gests that the larvae actually fit the description Saint Martin. of Cx. nigripalpus, a species that is sometimes found in crab holes as well (Belkin et al., 1970). Culex (Culex) bahamensis Dyar & Knab, 1906 Van der Kuyp’s adults do however resemble Culex bahamensis was collected in large num- the few available descriptions of Cx. habilita- bers at two brackish water sites on Sint tor (Dyar, 1928; Lane, 1953 [erroneously noted Maarten (Lowlands, 18°02’28.7“ N, 63°07’ as “habilitador” [sic]]; Bram, 1967). The fact 28.2” W, in saltwater rockpools; Guana Bay, that Cx. habilitator is present on many of the 18°01’54.6“ N, 63°01’25.9” W, in a puddle on the Lesser Antillean islands (Belkin & Heinemann, concrete driveway of an unfinished and aban- 1975, 1976; Schaffner, 2003) suggests that this doned mansion). species may be present on the Dutch Leeward This is in line with all the findings of Van Islands too. To determine whether Van der der Kuyp (1948, 1949, 1954), which are also Kuyp’s records really represent this species, a from brackish water. However, this species has reanalysis of the original material stored in the

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Smithsonian Institution is needed (National Culex (Culex) bisulcatus (Coquillett, 1906) Museum of Natural History, Washington D.C., Culex bisulcatus was synonymized with Cx. USA – NMNH). americanus (NeveuLemaire, 1902) by Dyar (1928), but restored by Stone (1967) as a valid Culex (Culex) nigripalpus Theobald, 1901 species. Berlin (1969a: 30–34) re-analyzed the Culex nigripalpus has been recorded for the material of Van der Kuyp and concluded that first time from the Dutch Leeward Islands in the material belongs to Cx. bisulcatus. Materi- our survey at two localities on Sint Maarten al from the Leeward Islands matches the topo- (2 ♀, 1 ♂, Rolandus Channel, 18°01’53.9“ N, typic material from Guadeloupe, except for 63°02’17.7” W, April 20th, 2018; 1 ♀, Belvedere, the number of setae on the 9th tergite lobe of 18°03’26.9“ N, 63°02’14.4” W, April 20th, 2018, the male genitalia, which are more numerous next to an open drain and small pond). on those of the Leeward Islands (Berlin, When Van der Kuyp sampled the Rolandus 1969a). Up to now, this taxonomic problem Channel in the late 1940s, Cx. nigripalpus was has not been addressed using modern genetic not observed (Van der Kuyp, 1953, 1954), but analysis. Due to a lack of genetic reference Cx. habilitator was recorded at this locality. material, we were unable to address this prob- The larvae of that species look very similar to lem in the current study. In this study, larvae those of Cx. nigripalpus. Therefore, Cx. nigri- of Cx. bisulcatus were only observed in bro- palpus may have been present during Van der meliads on Saba. The species was previously Kuyp’s inventory but was misidentified as Cx. also recorded on Sint Eustatius and Sint habilitator. Maarten (Van der Kuyp, 1948, 1949, 1953, 1954), but was not retrieved from these locations Culex (Culex) quinquefasciatus Say, 1923 despite considerable efforts. There are two Culex quinquefasciatus is strongly associated possible explanations for this. First, climato- with urbanization, as it prefers artificial con- logical conditions were suboptimal for this tainers and polluted groundwater as larval species during our visit. This may be an expla- habitats (Belkin et al., 1970). The species had nation for Sint Eustatius, where most of the been already introduced into the New World sampled phytotelmata were dry in compari- from Africa before 1800 (Belkin, 1962). As ex- son to the summer when they may be filled pected, Cx. quinquefasciatus was present in with water. Second, the number of bromeliads urban habitats on all three islands. Because of was strongly reduced due to urbanization and the complexity of the Cx. pipiens complex, of recent hurricanes on Sint Maarten (Richard- which Cx. quinquefasciatus is a member, we son et al., 2015), as we observed many brome- did not delve deeper into the identification of liads on fallen branches. Despite sampling this species on the Dutch Leeward Islands. All dozens of bromeliads on Sint Peter Hill and (sub)tropical populations from the New World the South Reward, the only remaining habitat have been considered to be Cx. quinquefascia- on Sint Maarten, no larvae were found. tus although Culex pipiens s.s. was also introduced to the Americas (Harbach, 2012). The Deinocerites magnus (Theobald, 1901) two lack clear morphological differences and Adults of De. magnus were collected in or interbreed within their non-native range close to crab holes at several localities on Sint (Cornel et al., 2012). Only a genetic study of Maarten. Van der Kuyp (1948, 1949, 1953, 1954) the Caribbean populations can reveal their identified this species as De. cancer, but it was identity. later identified as De. magnus by Adames

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(1971) after examining Van der Kuyp’s original portoricensis (as mentioned in the identifica- material. Deinocerites cancer has not been re- tion key by Belkin et al. (1970)). This may indi- corded from other islands of the Lesser Antil- cate that Saba hosts two Toxorhynchites spe- les (Gaffigan et al., 2019). cies. On Montserrat where these two species of Toxorhynchites occur, Tx. portoricensis oc- Psorophora (Grabhamia) pygmaea curs only in tree holes and Tx. guadeloupensis (Theobald, 1903) only in bromeliads (Belkin et al., 1970). To fur- Van der Kuyp (1953, 1954) recorded Ps. pyg- ther address this issue and identify the Saba maea from the Rolandus Channel on Sint species with absolute certainty, more refer- Maarten. During the 2018 survey, this species ence material and additional molecular work was not observed at this location, but was are required. found in shallow ponds on a flooded lawn in the Belvedere district, but only during the Overall shifts in mosquito community rainy season. The species is known to require composition on Sint Maarten between 1947 recently flooded plains for their eggs to hatch and 2018 (Belkin et al., 1970), which explains why they Due to its different geological history and were not observed during the dry season. Sint natural habitats, the mosquito fauna of Sint Maarten has lowlands with poorly drained Maarten contains a number of species indic- mineral soils, in strong contrast with the soils ative of lowland freshwater or brackish habi- of Sint Eustatius and Saba which consist of tats, including An. albimanus, Ps. pygmaea, better drained sandy-loam and are more steep and Cx. bahamensis. Well-draining soils, per- (Veenenbos, 1955). This makes it unlikely that manent high groundwater levels and an rainwater pools form long enough for the lar- abundance of land crabs provides the ideal vae of Ps. pygmaea to develop on Sint Eustati- habitat for De. magnus in almost all lowland us and Saba. areas on the island. In addition, during the 2018 survey, we observed Cx. nigripalpus and Toxorhynchites (Lynchiella) cf. guadeloupensis Ae. taeniornhynchus in these habitats, both (Dyar & Knab, 1906) of which we report new for the island of Sint During the 2018 survey, two Toxorhynchites Maarten. There were a number of other no- larvae were collected on Saba. A fourth instar table differences between 1947 and 2018. larva was sampled from a tree hole next to First, the ‘indicators of anthropogenic activi- Ladder Hill Road (17°37’49.9” N, 63°15’11” W) ty’ such as Ae. aegypti and Cx. quinquefascia- and an early instar larva was collected from a tus were very abundant and likely increased bromeliad next to Bud’s Mountain Trail (17°37’ due to a combination of urbanization as a N, 63°14’ W). The characteristics of these spec- result of major population growth (1951: imens are in accordance with the ones men- 1,478 inhabitants vs 2014: 40,552 inhabit- tioned in Augier et al. (2003). Therefore, we ants) and devastation by hurricanes. With assume that these specimens belong to Tx. increasing urbanization, most of the indige- guadeloupensis. This is in line with the finding nous forest is lost and consequently also spe- of a Tx. quadeloupensis larva in July 1949 by cies associated with these habitats, such as Van der Kuyp (1954) in a bromeliad on Mount Cx. bisulcatus. Scenery. However, both of our specimens have a ventral brush on the 10th segment consisting A tale of two islands of 9-10 tufts, which would suggest that the Despite the similarity in geology and natural specimens are more similar to those of Tx. history of the islandsDownloaded of Sint from Brill.com09/26/2021 Eustatius and 02:03:44AM via free access

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Saba, we observed a striking difference in the whereas this species was absent from the more current species communities compared with remote wells and cisterns on Saba. Overall, those in 1947. Although both ‘natural forest in- we conclude that the striking dissimilarity in dicators’ (Cx. bisulcatus and Ae. busckii) were mosquito species composition between the is- present on both islands during the 1947 survey lands of Sint Eustatius and Saba may be a com- (carried out in the same time of the year; Van bination of under-sampling, loss of suitable der Kuyp 1954), they are currently absent from habitat, and a difference in mosquito control Sint Eustatius but relatively abundant on Saba. approach. This difference may partly be due to limita- tions in sampling effort on Sint Eustatius, where we have not managed to sample all bro- Key to the adults meliads on the rim of the volcano and the sampling campaign lasted only one week during Morphological identification key to the adult the dry season. This makes it difficult to draw mosquitoes of the Dutch Leeward Islands. firm conclusions on the actual loss of species. Alternatively, it may be also be caused by a 1 Proboscis stiff; bent downwards; nar- more pronounced effect of climate change on rowed towards tip �� the natural forest on the volcano of Sint Eusta- �� Toxorhynchites cf. guadeloupensis tius (621 m asl) compared to Saba (872 m asl), – Proboscis flexible; not bent down- which may have caused the potential mosqui- wards; equal in width or swollen at tip to habitat to have shifted beyond the altitude ��2 of the volcano on Sint Eustatius. Indeed, we 2(1) Wings veins with spots of dark and have not observed any water filled phytotel- light scales. Scutellum evenly rounded mata on Sint Eustatius, whereas on Saba most on hind margin; with hairs evenly phytotelmata contained water. To test this hy- spaced. Female: palpi about as long as pothesis and to confirm if these species are re- the length of proboscis. Male: palpi ally absent from Sint Eustatius, additional club-shaped ��Anopheles albimanus sampling is required. The second aspect re- – Wing veins with only dark scales. Scu- garding the difference between these islands is tellum with three lobes on hind mar- the fact that adults of Ae. aegypti and Cx. quin- gin; each lobe bearing a separate group quefasciatus were collected much more fre- of hairs. Female: palpi less than half quently on the island of Sint Eustatius (100% the length of the proboscis. Male: tips of all collections on this island) than on Saba of palpi sometimes swollen, but never (3.6% of all collections on this island). This club-shaped ��3 may be due to the fact that the vector control 3(2) Postspiracular hairs present. Female: unit is able to visit every household on aver- apex of abdomen blunt, i.e. segment 7 age every 40 days on Saba which is not the case not narrowed, segment 8 short, but not on Sint Eustatius. Sint Eustatius has a popula- retracted ��4 tion twice the size of Saba, yet Saba’s vector – Postspiracular hairs absent. Female: control unit is twice the size of that in Sint Eu- apex of abdomen more or less pointed, statius, as a result of budgetary constraints. In i.e. segment 7 narrow, segment 8 short addition, Ae. aegypti has colonized some of the and retracted ��9 more remote fresh and brackish water wells 4(3) Prespiracular hairs present �� on Sint Eustatius, including one site which ��Psorophora pygmaea – Prespiracular hairs absent ��5 was previously inhabited by Cx. bahamensis, Downloaded from Brill.com09/26/2021 02:03:44AM via free access

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5(4) Tarsal segments of hind leg completely 12(11) Upperside of abdomen with large bas- dark scaled ��Aedes tortilis al white bands; each band distinctly – Tarsal segments of hind leg with at longer in the middle than at the sides. least some white scaled markings ��6 Mesepimeron with large patch of 6(5) Upperside abdomen dark without bas- scales medially �� al white bands ��Aedes busckii ��Culex quinquefasciatus – Upperside abdomen dark with basal – Upperside of abdomen unbanded or at white bands ��7 most narrow bands, shortest in the 7(6) Proboscis with median white ring...... middle. Mesepimeron without large �� Aedes taeniorhynchus patch of scales medially �� – Proboscis entirely dark, or with a few �� Culex nigripalpus light scales at tip ��8 13(11) Proboscis with a complete white ring 8(7) Mesonotum with two median grey in middle. Upperside of abdomen with stripes; sides with broad white stripes basal white bands, deepest in the mid- in first half of mesonotum; pattern of dle (forming triangular spots). Tibia of mesonotum pattern forming a lyre hind leg with white stripe on under- shape. Clypeus with white scales...... side. Female: palpi with white mark- ��Aedes aegypti ings, mesonotum with pattern of white – Mesonotum with one median white scales ��Culex bahamensis stripe; sides without white stripes on – Proboscis with a usually incomplete first half of mesonotum; pattern of white ring. Upperside of abdomen mesonotum never lyre shaped. Clype- with basal white bands, shortest in the us bare �� Aedes albopictus middle; sometimes absent. Tibia of 9(3) Antenna much longer than proboscis; hind leg without white stripe on un- flagellar segment 1 twice as long as derside. Female: palpi entirely dark clypeus and distinctly longer than seg- scaled, without white markings, me- ment 2 �� Deinocerites magnus sonotum without white scales �� – Antenna shorter than proboscis; flagel- ��Culex habilitator lar segment 1 of antenna subequal or shorter than clypeus and about the same length as second ��10 Key to the fourth-instar larvae 10(9) Thorax with at most with a few scales along sternopleuron (stp) bristles. Morphological identification key to the fourth Male: palpi about one third the length instar larvae of mosquitoes of the Dutch Lee- of proboscis �� Culex bisulcatus ward Islands. – Thorax with distinct scale patches on 1 Respiratory siphon absent; at least sternopleuron (stp). Male: palpi at some abdominal terga with seta 1 pal- least as long as proboscis ��11 mate ��Anopheles albimanus 11(10) Hind legs entirely dark scaled, without – Respiratory siphon present as a strong- distinct pale ring over joints of tarsal ly chitinized air-tube on segment 8; segments �� 12 seta 1 on abdominal terga never pal- – Hind legs with distinct pale ring over mate ��2 joints of tarsal segments, sometimes 2(1) Respiratory siphon without pecten very narrow �� 13 teeth; comb scales absent, replaced by Downloaded from Brill.com09/26/2021 02:03:44AM via free access

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a large sclerotized plate bearing hairs 11(10) Comb scale with a prominent single ��Toxorhynchites cf. guadeloupensis denticle, with strong preapical spines – Respiratory siphon with pecten teeth; on sides, giving it a trident like shape comb scales present ��3 ��Aedes aegypti 3(2) Respiratory siphon with at least three – Comb scale with a single denticle, tufts �� 4 with a lateral fringe of fine spicules – Respiratory siphon with only a single �� Aedes albopictus tuft �� 9 12(10) Saddle on segment 10 forms an incom- 4(3) Head widest at about the level of base plete ring; ventral brush with five or six of antennae; abdominal segment 10 pairs of hairs; comb scales long and with two separated sclerotized plates slender ��Aedes busckii �� Deinocerites magnus – Saddle on segment 10 forms a com- – Head widest in posterior half; abdomi- plete ring; ventral brush with seven to nal segment 10 with a single sclero- nine pairs of hairs; comb scale broad tized plate ��5 ��13 5(4) Setae of thorax and abdomen stellate 13(12) Saddle on segment 10 with small spic- ��Culex bisulcatus ules on caudal fifth. Lateral abdominal – Setae of thorax and abdomen not stel- hair (6) on segment 3 to 5 usually triple late �� 6 (double to 5-branched �� 6(5) Respiratory siphon with six aligned ��Aedes taeniorhynchus tufts; a single pair of anal gills �� – Saddle on segment 10 smooth on cau- �� Culex bahamensis dal fifth. Lateral abdominal hair (6) on – Respiratory siphon with three to four segment 3 to 5 usually single �� setae or tufts placed lineally, with one ��Aedes tortilis seta or tuft dorsally out of line; two pairs of anal gills ��7 7(6) Siphon index less than 5 �� Conclusion �� Culex quinquefasciatus – Siphon index at least 5.5 �� 8 Here we report on the results of a mosquito 8(7) Tufts on respiratory siphon single or survey of the Dutch Leeward islands (Sint double (apical tuft rarely triple �� Maarten, Sint Eustatius and Saba) carried out �� Culex nigripalpus in 2018 which was the first extensive survey – Tufts on respiratory siphon double or since 1949. Using a variety of collection meth- triple ��Culex habilitator ods, we observed two new disease vector spe- 9(3) Ventral brush of segment 10 covers al- cies for the island of Sint Maarten, Ae. taenio- most the full length of this segment �� rhynchus and Cx. nigripalpus, vectors for �� Psorophora pygmaea dog heartworm (Manrique-Saide et al., 2010) – Ventral brush of segment 10 covers and West Nile virus (Barrera et al., 2008), re- less than half of length of this segment spectively. One previously recorded species, ��10 Cx. habilitator was not observed. We did not 10(9) Comb scales arranged in a single row find Ae. albopictus. The species richness of ��11 the mosquito fauna of Sint Eustatius seems to – Comb scales arranged in multiple rows have decreased compared to previous surveys or a patch ��12 and is currently dominated by Ae. aegypti and Downloaded from Brill.com09/26/2021 02:03:44AM via free access

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Cx. quinquefasciatus, of which the former has References also colonized some of the more remote (even brackish) locations previously inhabited by the Adames, A.J. (1971) Mosquito studies (Diptera, Cu- native Cx. bahamensis. In contrast, the fauna licidae). XXIV. A revision of the crabhole mos- on Saba has remained quite similar compared quitoes of the genus Deinocerites. Contrib. Am. to the 1949 survey (Van der Kuyp, 1954), with Entomol. Inst. 7, 1–154. a species pool dominated by species charac Arnell, H.J. (1976) Mosquito Studies (Diptera, Cu- teristic of relatively undisturbed forests. Re- licidae) XXXIIL A Revision of the scapularis sults of this study emphasize the need for regu- group of Aedes (Ochlerotatus). Contrib. Am. En- lar species inventories of mosquitoes in the tomol. Inst. 13, 1–144. Caribbean. Augier, L.M., Juri, M.J.D. & Molina, G.A. (2003) Re- descripción de la larva y la pupa de Toxo- rhynchites (Lynchiella) guadeloupensis (Diptera: Culicidae). Rev. la Soc. Entomológica Argentina Acknowledgements 62, 99–106. Barrera, R., Bingham, A.M., Hassan, H.K., Amador, We are greatly indebted to a number of peo- M., Mackay, A.J. & Unnasch, T.R. (2012) Verte- ple without whom this study would not have brate hosts of Aedes aegypti and Aedes mediovit- been possible. We are particularly grateful to tatus (Diptera: Culicidae) in rural Puerto Rico. J. everyone on the islands for great logistical Med. Entomol. 49, 917–921. support, especially Clarisse Buma on Sint Eu- Barrera, R., Hunsperger, E., Muñoz-Jordán, J.L., statius and Randall Johnson on Saba. Special Amador, M., Diaz, A., Smith, J., Bessoff, K., Be- thanks to Delia Goilo from the Curaçao Bio- itran, M., Vergne, E., Verduin, M., Lambert, A. & medical & Health Research Institute and Em- Sun, W. (2008) Short report: First isolation of ily Khazan from the School of Natural Re- West Nile virus in the Caribbean. Am. J. Trop. sources and Environment at University of Med. Hyg. 78, 666–668. Florida for joining the expedition team for Bass, C.M. & Bass, D. (2011) Aquatic invertebrate one week and providing some indispens- community structure in water-filled bracts of able help. We thank Dr. Yoosook Lee, Dr. Travis Heliconia caribaea (Heliconiaceae) on Saba, Collier and Allison Weakley from the Vector West Indies. Living World, J. Trinidad Tobago Genetics Laboratory of the Department of F. Nat. Club 2011, 60–65. Pathology, Microbiology and Immunology of Belkin, J.N. (1962) The Mosquitoes of the South Pa- the University of California for sharing their cific (Diptera, Culicidae). Vols. 1 and 2. University species records from Saba. This study was sup- of California Press, California. ported by a donation by the Gieskes Strijbis Belkin, J.N. & Heinemann, S.J. (1975) Collection re- fund, the Leiden University LUSTRA+ scholar- cords of the project “Mosquitoes of Middle ship and the Saba Sea & Learn Foundation. America”. 3. Bahama Is. (BAH), Cayman Is. (CAY), We thank Menno Schilthuizen and one anon- Cuba (CUB), Haiti (HAC, HAR, HAT) and Lesser ymous reviewer for the useful comments. Antilles (LAR). Mosq. Syst. 7, 367–393. Belkin, J.N. & Heinemann, S.J. (1976) Collection records of the project “Mosquitoes of Middle Supplementary material America”. 4. Leeward Islands: Anguilla (ANG), Antigua (ANT), Barbuda (BAB), Monserrat Supplementary material is available online at: (MNT), Nevis (NVS), St. Kitts (KIT). Mosq. Syst. 8, https://doi.org/10.6084/m9.figshare.12085773 123–162. Downloaded from Brill.com09/26/2021 02:03:44AM via free access

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Making mosquito taxonomy useful: A stable RECEIVED: 20 JANUARY 2020 | REVISED AND classification of tribe Aedini that balances util- ACCEPTED: 31 MARCH 2020 ity with current knowledge of evolutionary re- EDITOR: R. VONK lationships. PLoS One 10, 1–26.

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