Journal of Vector Ecology
90
June 2015
Seasonal dynamics and habitat specificity of mosquitoes in an English wetland: implications for UK wetland management and restoration Jolyon M. Medlock and Alexander G.C. Vaux Medical Entomology and Zoonoses Ecology Group, MRA, Emergency Response Department, Public Health England, Porton Down, Salisbury, United Kingdom,
[email protected] Received 1 August 2014; Accepted 10 October 2014 ABSTRACT: We engaged in field studies of native mosquitoes in a Cambridgeshire Fen, investigating a) the habitat specificity and seasonal dynamics of our native fauna in an intensively managed wetland, b) the impact of water-level and ditch management, and c) their colonization of an arable reversion to flooded grassland wetland expansion project. Studies from April to October, 2010 collected 14,000 adult mosquitoes (15 species) over 292 trap-nights and ~4,000 pre-imaginal mosquitoes (11 species). Open floodwater species (Aedes caspius and Aedes cinereus, 43.3%) and wet woodland species (Aedes cantans/annulipes and Aedes rusticus, 32.4%) dominated, highlighting the major impact of seasonal water-level management on mosquito populations in an intensively managed wetland. In permanent habitats, managing marginal ditch vegetation and ditch drying significantly affect densities of pre-imaginal anophelines and culicines, respectively. This study presents the first UK field evidence of the implications of wetland expansion through arable reversion on mosquito colonization. Understanding the heterogeneity of mosquito diversity, phenology, and abundance in intensively managed UK wetlands will be crucial to mitigating nuisance and vector species through habitat management and biocidal control. Journal of Vector Ecology 40 (1): 90-106. 2015. Keyword Index: Wetlands, ecology, mosquitoes, Anopheles, Aedes, Culex.
INTRODUCTION One of the main challenges to adapting to climate change in the United Kingdom (UK) has involved the development of national and regional strategies to mitigate coastal and inland flooding through the provision of new wetlands. In an attempt to further increase the available habitat for wildlife to cope with changes in climate, existing wetlands are also being extended, new wetlands are being created, and failing wetlands are being restored. To address this, the Wetland Vision for England, sponsored by UK government departments and agencies and implemented by nongovernmental environmental organizations, has developed a clear vision to restore large parts of England back to wetland by 2050. Many of these strategies involve recreating wetland landscapes where wetlands had previously dominated, with plans to create new coastal aquatic habitats in eastern and southern England that mitigate rises in sea levels and tidal surges, or offset loss of European protected coastal habitat. Inland, in urban areas, new wetlands are often created as part of ecological mitigation for new housing developments. However, one of the greatest visions for wetland creation includes arable reversion to wetlands, such as the Great Fen project and Wicken Fen vision in Cambridgeshire. At the Great Fen, arable land adjacent to Woodwalton and Holme Fens has been purchased with the intention of extending the existing high-biodiverse wetlands to increase the wildlife value of the existing nature reserves and minimize wetland fragmentation, as well as to aid water storage. Primarily, the vision is to restore a lost wetland landscape, as well as to increase the available habitat for birds, rare plants, and invertebrates. This project is just one example of a number of wetland creation schemes in place across England. In addition to meeting wildlife goals, there are a multitude of benefits to creating new wetlands. They provide important
social, economic, and ecological services such as flood control, water quality improvement, carbon sequestration, and pollutant removal (Rey et al. 2012). Wetlands also have high aesthetic and recreational value that make wetland landscapes highly desirable for improving human well-being and in turn promote local rural economies through the increase in tourism and development of new settlements. There are few negatives associated with wetlands except for the prospects of nuisance biting flies and the potential for future insectborne disease transmission (Walton 2001, Chase and Knight 2003, Malan et al. 2009, Medlock and Vaux 2011). The risk posed by the latter has been heightened by the recent incursion of Culicoides midge-transmitted Bluetongue and Schmallenberg viruses of veterinary concern (Carpenter et al. 2013). In recent decades, England has been free of the transmission of mosquito-associated pathogens, although it is less than 100 years since malaria was endemic in coastal marsh and fenland parts of England (Dobson 1997). Furthermore, since the extensive emergence of West Nile virus (WNV) in North America beginning in 1999 (Petersen and Hayes 2008, Reisen 2013), a great deal of attention has focussed on the role of both native and non-native mosquitoes in the potential and actual transmission of diseases to humans in Europe (Medlock et al. 2005, Sambri et al. 2013). In the last five years, continental Europe has witnessed its own local and ongoing transmission of WNV to humans across the eastern and central Mediterranean region (Engler et al. 2013). European mosquitoes have also been involved in the transmission of vivax malaria in Greece (Danis et al. 2013), the emergence of African flaviviruses such as Usutu virus in central Europe (Calzolari et al. 2013), and the prospect of European transmission of Rift Valley fever virus by European mosquitoes remains a serious concern of European agriculture bodies (Chevalier 2013, Zeller et al. 2013). In addition, two other
Vol. 40, no. 1
Journal of Vector Ecology
arboviruses transmitted by European mosquitoes occur cyclically in Europe: Sindbis virus in Scandinavia (Ahlm et al. 2013) and Tahyna virus in central Europe (Hubalek et al. 2010), both of which cause human disease. Furthermore, the recent invasion of non-native invasive mosquitoes, such as Aedes albopictus, Aedes aegypti, and Aedes japonicus (Medlock et al. 2012, Schaffner et al. 2013), and their involvement in European transmission of dengue virus (Sousa et al. 2012) and chikungunya virus (Angelini et al. 2008), has raised the prospect of mosquitoes as a cause for public health concern in the UK and Europe. One of the challenges for wetland managers and entomologists involved with public health assessment is ensuring that existing and new wetlands are not a cause of concern for public health disease risk either now or in the future (Medlock and Vaux 2011). There have been very few studies that have assessed the importance of English wetlands as a source of nuisance or disease vector mosquitoes, and much of the published literature on British mosquitoes is now quite historical, and mostly concerned with species biology, rather than species ecology from a wetland manager perspective. Some progress has been made recently in understanding vector and nuisance issues associated with mosquitoes in new coastal (Medlock and Vaux 2013) and urban habitats (Medlock and Vaux 2014), but there remains a lack of clear field evidence for the role of newly created UK freshwater wetlands in exacerbating nuisance or disease issues, nor is there any practical guidance for wetland managers to mitigate such events (Medlock and Vaux 2011). Faced with an outbreak of a mosquito-borne arboviral infection in England, possibly associated with a wetland system or a large-scale flooding event, the UK contingency plan for WNV promotes the use of insecticidal control. The challenge is that there is a dearth of evidence to prove that wetlands actually harbor nuisance or vector species, and little work has been done to classify which of the putative vector species are associated with specific wetland types. Furthermore, given that British wetlands are heavily managed environments, there may be wetland management strategies, such as scrub clearance, ditch brinking and slubbing, and water level management that might prove more successful in affecting mosquito numbers than broad-scale insecticidal control. During an outbreak response phase, what advice should wetland managers be given to manage mosquitoes using natural processes, and from a government policy perspective, is there evidence to state categorically that wetlands present no human disease risk either now or in the future? This study aims to begin to address this knowledge gap. The Great Fen project in Cambridgeshire presents an excellent opportunity to assess not only the role of different wetland communities and different aquatic wetland types in supporting mosquitoes in an extant high-biodiverse wetland, but also to investigate the impact of certain wetland management (ditch brinking and slubbing) and wetland expansion initiatives (arable reversion to wet grassland) on British mosquitoes. The objectives of this study were to: 1. Investigate the seasonality and abundance of pre-imaginal and adult mosquito populations associated with a range of aquatic habitats within an established freshwater wetland in England, using Woodwalton Fen and the Great Fen as examples. 2. Describe how hydrological changes associated with the
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management of different wetland types might affect the lifehistories (phenology and abundance) of the different mosquito species. 3. Understand the importance of ditch management (brinking and slubbing) and maintaining ditch water levels on mosquitoes in permanent aquatic habitats, particularly during drought conditions. 4. Begin to understand the impact on mosquitoes of arable reversion to wet grassland as part of wetland expansion. MATERIALS AND METHODS Study site The Cambridgeshire Fens provide an ideal location for studies on freshwater wetland systems, home to some of the oldest nature reserves in England. They are also the location of extensive wetland expansion, and hence the Great Fen (which includes Woodwalton Fen) provides an opportunity to study mosquitoes in a natural well-established freshwater wetland system, with active and regular wetland management and wetland expansion schemes. Field sampling was conducted at Woodwalton Fen National Nature Reserve (Cambridgeshire; 208 ha; 52º27’N, 0º11’W) and the adjacent farmland that forms part of the 3,700 ha Great Fen. Woodwalton Fen is managed to create a diverse range of habitat types within various seral stages represented by tall fen (NVC classifications S4, 24, 26), fen meadow (M22, M24), heath/mire (M25), rush pasture (MG10), swamp (S4), open water, woodland, and willow carr (Rodwell et al. 1995). The northern third of the reserve is dominated by swamp vegetation, composed mostly of reedbed and tall fen [reedbed community]. The middle section is dominated by tall fen and a managed gridded ditch system [fen and ditch community]. The southern half of the reserve is composed of four parts: willow carr, fen meadow, acid heath and open meres, with all field studies focussed on the willow carr [wet woodland community] (Figure 1). Lying to the west of Woodwalton Fen is an area of wetland expansion. Prior to the Great Fen project, all of this area was arable farmland. However, the northern part is now composed of ‘flooded grassland,’ the central part is newly established ‘grassland,’ and the southern third remains ‘arable’ land. Field studies on the adult mosquito populations were directed towards these six different communities: wet woodland (WW), fen and ditch (FD), reedbed (RB), flooded grassland (FG), grassland (GR), and arable (AR), with WW and AR, FD and GR, RB and FG lying adjacent on a 3 by 2 matrix (Figure 1). Sampling the adult population Adult mosquitoes were surveyed to investigate the diversity, phenology, and abundance of adult mosquitoes across the six communities. Adult females were trapped over four nights every two weeks for up to 14 weeks from April to October, 2010 using the Liberty Plus Mosquito Magnet trap (Midgetech). This trap produces CO2 and heat and is baited with an octenol-based lure. Owing to concerns over the impact of light traps on rare moth species and the logistical difficulty of accessing remote sites with dry ice, no other adult mosquito traps were employed. Therefore, it was anticipated that ornithophagic species (such as Culex pipiens s.l./Cx. torrentium) would be undersampled. One trap was placed in each of the six communities, with adult mosquitoes collected
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Journal of Vector Ecology
after each four-night sampling period, and identified using taxonomic keys (Snow 1990, Schaffner et al. 2001). Occasionally, for various logistical reasons, it was not possible to sample all sites in all weeks. Where this was the case, this is noted in the results section. No attempt was made to separate Aedes cantans from Aedes annulipes (hereafter Ae. cantans), Aedes cinereus from Ae. geminus (hereafter Ae. cinereus), Cx. pipiens s.l. from Cx. torrentium (hereafter Cx. pipiens/torrentium), or to identify the members of the An. maculipennis complex using molecular techniques (hereafter An. maculipennis s.l.). Ecologically, the difference between these species groups is not considered important in the UK, and wild caught specimens do not permit accurate differentiation using morphological techniques (Linton et al. 2005, Medlock and Vaux 2009, 2011, Hesson et al. 2013). Two mean abundance calculations were derived both for total mosquito numbers and for each species: a) mean abundance per night for each survey week (X /nw), whereby total numbers of mosquitoes collected were divided by the number of survey nights each week, and the mean abundance per night across the entire survey season (X /ns). The best predictors for habitat specificity and seasonal activity for each species were identified using a Poisson log generalized linear model (GLM) using Stata and the principal predictor variable, and R2 was determined using a stepwise regression analysis using Minitab. Species were also classified to functional groups in accordance with Schafer et al. (2004) to identify the main functional groups for each community These functional groups were classified by aspects of their life cycle: oviposition site (water:land), overwintering stage (egg:larva:adult), known blood host preference (mammals:birds), and reported voltinism (uni-, multivoltine). Diversity and evenness indices were calculated for each community using Simpson’s diversity index (1-D) and ShannonWeiner Index (H’) to assess species dominance. Data on mean (Tm), maximum (Tx), and minimum (Tn) daily temperature, and daily rainfall was acquired from the local Ramsey weather station (5 km away). Sampling the immature population Pre-imaginal sampling was conducted at a range of aquatic habitats (Figure 1, Table 4) to determine which mosquito species are associated with different aquatic habitats and, where possible, calculate for each aquatic habitat the mean density of immatures per liter of water sampled across the season (Ls) and the highest density of immatures per liter recorded during the season (Lp). The first objective of the immature sampling involved surveying permanent ditches in Woodwalton Fen every two weeks to assess the impact of ditch management on mosquito abundance and diversity. Sixteen ditches were chosen according to their management type by whether the ditches had been slubbed (mechanically dug out and de-silted to prevent drying up) in the survey year (Y0) or the year before (Y-1), and brinked (mechanical cutting of marginal vegetation) or not in the survey year. The surveyed ditches included two ditches that had dried (Ddry) during the survey year (Y0), seven that remained wet and were brinked (Dw /b) during the survey year (Y0), and seven that remained wet and were not brinked (Dw /nb) during the survey year. At each of the 16 sampling points each ditch was sampled
June 2015
Figure 1. Schematic map of Woodwalton fen (RB=reedbed, FD=fen/ditch, WW=wet woodland) and Great Fen habitats (FG=flooded grassland, GR=grassland, AR=arable), with locations of sampling points: red dots=adult traps, blue triangle=ditches, black star=wet woodland pools/ditch, green diamond=flooded grassland/wet fen, yellow circle=reedbed, grey circle=mere. 20 times using a standard 0.5 liter dipper. The abundance of immature mosquitoes and all other invertebrates or reptiles/fish in the ditches were recorded at each sample. The impact of brinking (Y0), slubbing (Y-1, Y0), and drying (Y0) on the abundance of anophelines and culicines was determined using a Poisson log generalized linear model in Stata, and principal predictor variables and association with other invertebrates were identified using a stepwise regression analysis in Minitab. The second objective involved immature sampling every two weeks at the following aquatic habitats: two sampling points in the reedbed (Rb wet, Rb dry), two sampling points at wet woodland pools (WP dry), one sampling point at a wet woodland ditch (WP wet), two sampling points in meres, one sampling point in wet fen, at six agricultural ditches (GR community), and in flooded grassland (FG community). At each sampling point, aquatic habitats were sampled 20 times using a standard 0.5 liter dipper, except in the woodland pools, woodland ditch, and flooded grassland which were sampled 12 times using 0.25 liter dips. Larvae were identified to species and stage (I-III, IV instars) using taxonomic keys (Snow 1990, Schaffner et al. 2001) and pupae reared and identified as adults. These data were used qualitatively to understand the predilection of different mosquitoes to different aquatic habitats, and to assist in explaining any variance in abundance of adult mosquitoes in the six different communities.
Journal of Vector Ecology
Vol. 40, no. 1 RESULTS
Weather April was warm, with Tx of 22° C and Tm of 14° C in late April. Early/mid May was cooler (Tm 5-10° C) with three nights of Tn 30° C), except for a cool late June. Highest Tx (33.9° C) and Tm (22.3° C) were recorded in early July, with a steady decline from early August onwards, with Tn 110 mm of rain/month, with >70 mm between 23 and 27 August. A drier period followed (33-36 mm/month in September/October) with the majority of rain (25 mm) between 29 September-2 October. Consequently, all transient habitats dried out during the summer, re-wetting from late August and remaining wet through the autumn. Adult mosquito population data by wetland community Adult mosquito traps were run over 292 trap nights between April-October, 2010 (weeks 16-42) across the six different communities. Adult mosquitoes from 15 different species groups were collected and identified, with data on total numbers of mosquitoes and mean abundance presented for the principal species in Figure 2. The most abundant species were Aedes caspius (n=3,107, 22.2%), Aedes cinereus (2,978, 21.2%), Aedes cantans
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(2,750, 19.6%), Aedes rusticus (1,799, 12.8%), Coquillettidia richiardii (1,589, 11.3%), Anopheles claviger (668, 4.7%), and Culiseta annulata (614, 4.3%). All other species (Anopheles maculipennis s.l., Culiseta fumipennis, Culiseta morsitans, Culex pipiens/torrentium, Aedes geniculatus, Aedes detritus, Aedes flavescens and Aedes punctor) were less abundant (520, 3.7%). Five of the six communities recorded nine to ten species, with 15 in the wet woodland (Table 1). The dominance of particular species in WW (Ae. cantans and Ae. rusticus) and FG (Ae. cinereus and Ae. caspius) communities were indicative of low Simpson’s Diversity and Shannon-Weiner indices and evenness score (Table 1), with the highest mosquito diversity and evenness in the FD and AR communities where mean densities of mosquitoes were the lowest. The highest ns (mean densities/night over season) occurred in the WW (99.8 /ns), RB (70.6 /ns), and FG (42.1 /ns). Much lower overall adult mosquito densities were reported in the GR (27.6 / ns), FD (26.1 /ns), and AR (14.1 /ns). Similarly, the highest peak density (nw) varied hugely between communities and was again higher in WW (469.8 /nw), RB (438.3 /nw), and FG (216.8 /nw), with lower peak densities in the GR (171.8 /nw), FD (98 /nw), and AR (81.3 /nw) (Table 1). Adult activity over the season was distinctly bimodal (Figure 3) with most species active (and peaking) in week 26, with a second peak in weeks 38-40 dominated by Ae. cinereus and Ae. caspius. Wet woodland. Adults from 15 species (Figure 3a) were caught in WW over 48 nights (12 weeks). Adult density peaked in week 26, with minimal activity after week 32 although there was no trap
Table 1. Summary of adult mosquito trap data by wetland community and by species. Species counts with >100 individuals trapped by community are highlighted in bold. Community Survey weeks (Trap nights) Species richness (S) Simpson’s diversity index (1-D )
Woodland
Fen/ditch
Reedbed
Flooded grassland
Grassland
Arable
12 (48)
12 (48)
14 (56)
13 (52)
11 (44)
11 (44)
15
10
10
9
10
10
1.37
1.98
1.57
0.99
1.31
1.69
Shannon Weiner Index (H’)
0.67
0.85
0.73
0.56
0.57
0.78
Evenness
0.51
0.86
0.68
0.45
0.57
0.73
Functional groups
9
7
7
6
7
6
Total number of mosquitoes
4788
1253
3955
2187
1212
630
Mean mosquitoes/night (SE)
99.75±37.9
26.1±8.8
70.63±34.6
42.06±17.6
27.55±15.5
14.32±7.1
Peak mean mosquitoes/night
469.8
98
438.3
216.8
171.8
81.3
Aedes cinereus Meigen
Numbers of adult mosquitoes trapped (Mean abundance per night across the season for each community, ns)
Anopheles claviger Meigen
1 (0.02)
260 (5.42)
1,547 (27.6)
1,145 (22)
23 (0.52)
2 (0.04)
123 (2.6)
209 (4.35)
290 (5.2)
27 (0.52)
18 (0.41)
1 (0.02)
23 (0.41)
3 (0.06)
3 (0.07)
2 (0.04)
143 (3)
200 (3.6)
19 (0.36)
55 (1.25)
54 (1.2)
584 (12.2)
214 (4.46)
396 (7.1)
90 (1.7)
105 (2.39)
200 (4.5)
1 (0.02)
2 (0.04)
6 (0.1)
4 (0.08)
6 (0.13)
An. maculipennis s.l. Meigen
4 (0.08)
Culiseta annulata (Schrank)
143 (3)
Culiseta fumipennis (Stephens)
6 (0.13)
Culiseta morsitans (Theobald) Coquillettidia richiardii (Ficalbi) Culex pipiens L. /torrentium Martini Aedes geniculatus (Olivier)
1 (0.02)
17 (0.4) 2,174 (45.3)
195 (4.06)
144 (2.6)
7 (0.13)
154 (3.5)
76 (1.7)
1 (0.02)
31 (0.65)
1,249 (22.3)
884 (17)
768 (17.5)
174 (3.9)
Aedes detritus (Haliday)
27 (0.6)
71 (1.48)
74 (1.3)
8 (0.15)
40 (0.9)
38 (0.8)
Aedes flavescens (Müller)
2 (0.04) 26 (0.5)
Aedes cantans (Meigen) Aedes caspius (Pallas)
Aedes rusticus (Rossi)
1,532 (31.9)
121 (2.52)
Aedes punctor (Kirby)
172 (3.6)
7 (0.15)
40 (0.9)
80 (1.8) 3 (0.07)
Journal of Vector Ecology
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June 2015
Seasonal adult mosquito abundance Ae. cantans Ae. caspius Cq. richiardii Ae. cinereus Ae. rusticus An. claviger Cs. annulata
120
Adults/trap night
100 80 60 40 20 0 16
18
20
22
24
26
28
30
32
34
36
38
40
42
Weeks
Figure 2. Mean (SE) abundance by trap night of adult mosquitoes across the six wetland communities. Only data for the principal seven mosquito species are shown. Week numbers refer to the following dates: 16 (19-23 Apr), 18 (3-7 May), 20 (17-21 May), 22 (31 May-4 Jun), 24 (14-18 Jun), 26 (28 Jun-2 Jul), 30 (26-30 Jul), 32 (9-13 Jul), 34 (23-27 Jul), 36 (610 Sep). 38 (20-24 Sep), 40 (4-8 Oct), and 42 (18-22 Oct). data for weeks 40-42, and little activity was expected given low abundance in week 38 cf. other traps. Ae. cantans (45.4%, 45.3 /ns) and Ae. rusticus (32%, 31.9 /ns) dominated the catch supplemented by Cq. richiardii (12.2%, 12.2 /ns), Ae. punctor (3.6%, 3.6 /ns), Cs. annulata (3%, 3 /ns), and An. claviger (2.6%, 2.6 /ns). During weeks 18-20, Ae. punctor dominated (75% week 18, 27.75 /nw) but was absent from week 22 onwards. Ae. detritus (0.6 /ns), Ae. geniculatus (0.4 /ns), Cs. fumipennis (0.1 /ns), An. maculipennis s.l. (0.08 /ns), Ae. flavescens (0.04 /ns), Ae. cinereus, Cs. morsitans, Cx. pipiens/ torrentium, and Ae. caspius (all 0.02 /ns) were also caught. Fen/ditch. Adults from ten species (Figure 3b) were caught in FD over 48 nights (12 weeks). Adult density was bimodal, peaking in weeks 26-28 and 40. No data are available for weeks 36-38. Four species dominated equally: Ae. cinereus (20.8%, 5.4 /ns), Cq. richiardii (17.1%, 4.5 /ns), An. claviger (16.7%, 4.4 /ns), and Ae. cantans (15.6%, 4.1 /ns), although their active period differed. Adult densities were low from weeks 16-24, with a notable early peak of Ae. rusticus in week 20 (15.5 /nw). In week 26, densities peaked (76 /nw), dominated by Cq. richiardii (37%, 28.3 /nw) and Ae. cantans (29%, 22 /nw), with low numbers of seven other species including An. claviger (8.3 /nw), Ae. detritus (6.3 /nw), and Ae. rusticus (6.3 /nw). Cq. richiardii and Ae. cantans densities dominated (weeks 26-30, 56-70%) but declined through to week 34 with Ae. cantans again caught in October (2.8 /nw). During weeks 40-42, a second
higher peak of activity (98 /nw) was dominated by Ae. cinereus (51 /nw), An. claviger (18.3 /nw), and Cs. annulata (22 /nw). An. claviger was caught throughout with modest peaks in week 18 (5.3 /nw) and weeks 26-32 (8.3 /nw) and a larger peak in week 40 (18.3 / nw). Ae. punctor (0.2 /ns) and Cx. pipiens/torrentium (0.04 /ns) were also caught in low numbers. Reedbed. Adults from ten species (Figure 3c) were caught in RB over 56 nights (14 weeks). The catch was dominated by Ae. cinereus (39.1%, 28 /ns) and Ae. caspius (31.6%, 22 /ns), supplemented by Cq. richiardii (396, 7 /ns), An. claviger (290, 5 / ns), Cs. annulata (200, 4 /ns), and Ae. cantans (144, 3 /ns). Adult densities were bimodal, peaking in week 26 (275 /nw) and week 38-40 (438 /nw). Prior to week 26, activity was low (
