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Pre-imaginal black fly assemblages in streams of Eastern Spain: environmental and substrate requirements

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A growing interest in the importance of simuliids in health and animal welfare in certain areas in Europe, such as around the Mediterranean basin, together with the fact that there is fragmentary ecological information on the pre-imaginal stages of these dipterans has led to the need to carry out further research. We studied the abundance and distribution of pre-imaginal stages—mainly the pupae—of simuliid species, and examined their assemblages in relation to environmental gradients identified in Mediterranean basins of eastern Spain. We report a total of 21 black fly species from the set of studied streams, where largely the most common species were Simulium (Simulium) intermedium and Simulium (Simulium) ornatum, two species of medical and veterinary concern. We found that pre-imaginal simuliid assemblages were strongly related to elevation, water temperature and turbidity, dissolved oxygen concentration and water velocity. The analysis of the optima and tolerances for these environmental factors suggests differences in ecological requirements of the pre-imaginal stages of the reported simuliid species. Likewise, it was found that the pupae of some species were strongly associated with specific substrates. We hope that our research results on autoecology of black fly species will contribute to the improvement of pest management programs.
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PRIMARY RESEARCH PAPER
Pre-imaginal black fly assemblages in streams of Eastern
Spain: environmental and substrate requirements
David Lo
´pez-Pen
˜a.Eduardo M. Garcı
´a-Roger .Ricardo Jime
´nez-Peydro
´
Received: 6 November 2019 / Revised: 5 February 2020 / Accepted: 11 February 2020 / Published online: 27 February 2020
ÓSpringer Nature Switzerland AG 2020
Abstract A growing interest in the importance of
simuliids in health and animal welfare in certain areas
in Europe, such as around the Mediterranean basin,
together with the fact that there is fragmentary
ecological information on the pre-imaginal stages of
these dipterans has led to the need to carry out further
research. We studied the abundance and distribution of
pre-imaginal stages—mainly the pupae—of simuliid
species, and examined their assemblages in relation to
environmental gradients identified in Mediterranean
basins of eastern Spain. We report a total of 21 black
fly species from the set of studied streams, where
largely the most common species were Simulium
(Simulium) intermedium and Simulium (Simulium)
ornatum, two species of medical and veterinary
concern. We found that pre-imaginal simuliid assem-
blages were strongly related to elevation, water
temperature and turbidity, dissolved oxygen
concentration and water velocity. The analysis of the
optima and tolerances for these environmental factors
suggests differences in ecological requirements of the
pre-imaginal stages of the reported simuliid species.
Likewise, it was found that the pupae of some species
were strongly associated with specific substrates. We
hope that our research results on autoecology of black
fly species will contribute to the improvement of pest
management programs.
Keywords Ecological gradients Mediterranean
streams Optima Simuliidae Spain Tolerance
Introduction
Black flies, also known as simuliids (Diptera: Simuli-
idae), are a relatively homogeneous family within
nematoceran dipterans, and ubiquitous to flowing
water (Currie & Adler, 2008). They are holometabo-
lous insects with pre-imaginal developmental stages
(i.e., larvae and pupae) settling in a variety of
submerged substrates in running waters, where they
can attain very high population densities of more than
500,000 individuals per m
2
(Palmer, 1994) and feed by
filtering particles of organic matter dragged by water
flow (Adler & McCreadie, 1997; Currie & Adler,
2008). Their high abundance means that simuliid
larvae and pupae are a source of food for many
Handling editor: Vero
´nica Ferreira
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10750-020-04206-0) con-
tains supplementary material, which is available to authorized
users.
D. Lo
´pez-Pen
˜a(&)E. M. Garcı
´a-Roger
R. Jime
´nez-Peydro
´
Institut Cavanilles de Biodiversitat i Biologia Evolutiva,
Universitat de Vale
`ncia (Estudi General), C/ Catedra
´tic
Jose
´Beltra
´n Martı
´nez, 2, Paterna, 46980 Valencia, Spain
e-mail: David.Lopez@uv.es
123
Hydrobiologia (2020) 847:1521–1538
https://doi.org/10.1007/s10750-020-04206-0(0123456789().,-volV)(0123456789().,-volV)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... The ecological characterization of blackfly breeding habitats has been intensified in Europe since the 1980s (Hansford & Ladle, 1979;Rivosecchi, 1986;Leclercq, 1987;Ignjatović-Ćupina et al., 2006) and in the north of Africa (Arigue et al., 2016;Belqat et al., 2018), but there is still a paucity of data concerning some European regions, such as the Mediterranean region. This is especially true in Spain, where populations of pest species including Simulium (Boophthora) erythrocephalum (De Geer, 1776), S. (Simulium) ornatum (Meigen, 1818), S. (S.) reptans (Linnaeus, 1758), S. (Wilhelmia) equinum (Linnaeus, 1758), S. (W.) lineatum (Meigen, 1804) and S. (W.) pseudequinum (Séguy, 1921), have recently increased their population sizes and geographical ranges and have thus become an emerging issue of public health and veterinary concern (López- Peña & Jiménez-Peydró, 2017;López-Peña et al., 2020), although the increase in their annoyance to humans may be explained by other factors such as increasing anthropophagic tendencies, changes in species compositions, decreased tolerance by people, increased knowledge resulting in more frequent reporting of the problem, etc. ...
... This directly targets one of the most challenging questions in biological control regarding whether natural antagonists provide enough limitation of the abundance of a pest due to the effects of competition for a shared resource, in this case substrate availability, or not. Previous studies have suggested no particular substrate preference for the set of species studied here (López-Peña et al., 2020), so competition may occur for any empty space on the riverbed. ...
... This result is consistent with the pupal habitat analysis of the local abiotic variables. Previous studies have highlighted the role of both meteorological and topographic factors, such as temperature and elevation, in shaping blackfly assemblages (McCreadie & Adler, 2006Ya'cob et al., 2016;López-Peña et al., 2020), however we did not include elevation in the set of variables used in the CCA as it was included in the dataset of abiotic variables and it showed a high negative correlation with annual average temperature (R 2 > 0.8, P value <0.001). Regarding the other landscape variables, our results suggest that breeding sites of S. (W.) equinum are positively associated with the presence of pig farms within a radius of 35 km around sampling sites, whereas those of S. (S.) reptans were found closer to cattle farms and within shorter distances from them. ...
Article
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Geographical distribution and abundance of the pupae of six blackfly species of medical and veterinary concern were studied in eastern Spain according to three different sets of explanatory variables including in-stream variables, both (i) abiotic (i.e., physicochemical) and (ii) biotic (i.e., richness and abundance of either taxonomically or ecologically close related taxa), as well as (iii) meteorological and landscape variables. The results showed specific habitat requirements for pupation in Simulium (Boophthora) erythrocephalum (De Geer, 1776) and Simulium (Wilhelmia) equinum (Linnaeus, 1758), two of the six species studied regarding elevation and temperature. While the rest of the species showed a certain degree of ecological overlap, co-occurrence was in general low, which suggested that antagonistic biotic factors may be important in structuring blackfly assemblages. In effect, biotic predictors explained a high proportion (50%–70%) of the variability in the abundance of the pupae of the most generalist blackfly species, although further studies are needed to disentangle the sign of interspecific interactions. At the landscape level, S. (W.) equinum and S. (W.) pseudequinum Séguy, 1921 breeding habitats were associated with the presence of pig farms, and S. (Simulium) reptans (Linnaeus, 1758) and S. (B.) erythrocephalum with the presence of cattle.
... Finally, simuliid species with obligate hematophagy of biomedical and veterinary importance [27] such as S. erythrocephalum are generalist species regarding the type of habitat in which they develop, Therefore, these species are capable of tolerating a wide range of ecological conditions. Under this premise and given the current climate change scenario in which certain authors and institutions predict a decrease in coldwater river habitats and greater environmental variability [28], it would be expected that the resulting conditions would favor the distribution and colonization of S. erythrocephalum to new geographic areas, increasing its harm to the well-being of citizens. ...
... In this way, the knowledge of the bioecology of the species will play a crucial role when it comes to implementing treatment plans for preimaginal states, minimizing the sizes of their populations and reducing their incidences in public health. In the case of S. erythrocephalum, it is important to know that it is a species whose preimaginal development optimum is 20°C, tolerates values higher than 25°C, shows a narrow range of altitudinal tolerance with its optimum around 75 meters above sea level (masl), so that its distribution in the Valencian Autonomous Region is restricted to elevations between 5 and 240 masl [27]. Likewise, some authors ecologically described this species as preferring lentic and warm waters typical of the middle and lower sections of rivers [30]. ...
Article
Full-text available
The presence and distribution of Simulium erythrocephalum (De Geer, 1776) in the Valencian Autonomous Region is analyzed, an arthropod of medical-sanitary importance due to the marked anthropophilic characteristics exhibited and the tendency to carry out massive attacks. The increasing incidence registered in certain areas as a consequence of their hematophagy, and the meager availability of epidemiological, fauna, bioecological, and distribution data, have led to this study. A field study of 137 samplings was carried out from 2013 to the present in the 14 hydrographic basins of the Valencian Autonomous Region. The study variables were the presence or absence of preimaginal states, environmental and physical-chemical parameters of the water, bite data from the Generalitat Valenciana, population density and incidence of bites by municipality, and geographic location of the population areas. A scarce and reduced presence of the aforementioned species is revealed in the study area. Risk maps of human populations near the detected breeding areas are provided, and the epidemiological interest is discussed due to its vector capacity to transmit pathogens that cause disease. The number of bites registered between 2015, 2016, 2017, and 2018 in the seven health departments involved is provided. The general trend toward an increase in the number of cases is observed year after year, where the highest peaks in the number of cases coincide with the months of June, July, and August, and eventually, September and October. Surveillance and control programs to minimize the problem in the Spanish health system are needed.
... Finally, simuliid species with obligate hematophagy of biomedical and veterinary importance [27] such as S. erythrocephalum are generalist species regarding the type of habitat in which they develop, Therefore, these species are capable of tolerating a wide range of ecological conditions. Under this premise and given the current climate change scenario in which certain authors and institutions predict a decrease in coldwater river habitats and greater environmental variability [28], it would be expected that the resulting conditions would favor the distribution and colonization of S. erythrocephalum to new geographic areas, increasing its harm to the well-being of citizens. ...
... In this way, the knowledge of the bioecology of the species will play a crucial role when it comes to implementing treatment plans for preimaginal states, minimizing the sizes of their populations and reducing their incidences in public health. In the case of S. erythrocephalum, it is important to know that it is a species whose preimaginal development optimum is 20°C, tolerates values higher than 25°C, shows a narrow range of altitudinal tolerance with its optimum around 75 meters above sea level (masl), so that its distribution in the Valencian Autonomous Region is restricted to elevations between 5 and 240 masl [27]. Likewise, some authors ecologically described this species as preferring lentic and warm waters typical of the middle and lower sections of rivers [30]. ...
... Finally, simuliid species with obligate hematophagy of biomedical and veterinary importance [27] such as S. erythrocephalum are generalist species regarding the type of habitat in which they develop, Therefore, these species are capable of tolerating a wide range of ecological conditions. Under this premise and given the current climate change scenario in which certain authors and institutions predict a decrease in coldwater river habitats and greater environmental variability [28], it would be expected that the resulting conditions would favor the distribution and colonization of S. erythrocephalum to new geographic areas, increasing its harm to the well-being of citizens. ...
... In this way, the knowledge of the bioecology of the species will play a crucial role when it comes to implementing treatment plans for preimaginal states, minimizing the sizes of their populations and reducing their incidences in public health. In the case of S. erythrocephalum, it is important to know that it is a species whose preimaginal development optimum is 20°C, tolerates values higher than 25°C, shows a narrow range of altitudinal tolerance with its optimum around 75 meters above sea level (masl), so that its distribution in the Valencian Autonomous Region is restricted to elevations between 5 and 240 masl [27]. Likewise, some authors ecologically described this species as preferring lentic and warm waters typical of the middle and lower sections of rivers [30]. ...
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The presence and distribution of Simulium erythrocephalum (De Geer, 1776) in the Valencian Autonomous Region is analyzed, an arthropod of medical-sanitary importance due to the marked anthropophilic characteristics exhibited and the tendency to carry out massive attacks. The increasing incidence registered in certain areas as a consequence of their hematophagy, and the meager availability of epidemiological, fauna, bioecological, and distribution data, have led to this study. A field study of 137 samplings was carried out from 2013 to the present in the 14 hydrographic basins of the Valencian Autonomous Region. The study variables were the presence or absence of preimaginal states, environmental and physical-chemical parameters of the water, bite data from the Generalitat Valenciana, population density and incidence of bites by municipality, and geographic location of the population areas. A scarce and reduced presence of the aforementioned species is revealed in the study area. Risk maps of human populations near the detected breeding areas are provided, and the epidemiological interest is discussed due to its vector capacity to transmit pathogens that cause disease. The number of bites registered between 2015, 2016, 2017, and 2018 in the seven health departments involved is provided. The general trend toward an increase in the number of cases is observed year after year, where the highest peaks in the number of cases coincide with the months of June, July, and August, and eventually, September and October. Surveillance and control programs to minimize the problem in the Spanish health system are needed.
... Our results also illustrate the broad tolerance to water current velocity conditions of taxa such as S. rubzovianum and S. intermedium s.l. (Gallardo-Mayenco and Toja 2002;L opez-Peña et al. 2020), and provide evidence that S. angustitarse and S. trifasciatum are found across the widest ranges of current velocities. For those taxa, common in this study and that of L opez- Peña et al. (2020) in the Iberian Peninsula, for which more ecological information is available, the rank distribution regarding water velocity was quite similar (Spearman's r ¼ 0.636). ...
... (Gallardo-Mayenco and Toja 2002;L opez-Peña et al. 2020), and provide evidence that S. angustitarse and S. trifasciatum are found across the widest ranges of current velocities. For those taxa, common in this study and that of L opez- Peña et al. (2020) in the Iberian Peninsula, for which more ecological information is available, the rank distribution regarding water velocity was quite similar (Spearman's r ¼ 0.636). Simulium lineatum was found in higher occurrence at lower values of TDS (Figure 5b), while in L opez-Peña et al. (2020), this was found to be the case for S. carthusiense (unrecorded in the UK), while S. equinum showed the widest TDS range but in L opez-Peña et al. (2020), this was true (for turbidity) of S. bezzi (unrecorded in the UK). ...
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Data on pre-imaginal stages of blackflies obtained in southern England during the summer and early autumn of 2020 were supplemented by additional surveys and analysed in relation to environmental factors. Fourteen taxa from 29 locations were recorded. Of these, seven are of medical and/or veterinary importance: Simulium (Wilhelmia) equinum (Linnaeus, 1758), S. (Boophthora) erythrocephalum (De Geer, 1776), S. (Simulium) intermedium Roubaud, 1906 sensu lato (s.l., a complex of species), S. (W.) lineatum (Meigen, 1804), S. (S.) morsitans Edwards, 1915, S. (S.) noelleri Friederichs, 1920 and S. (S.) ornatum (Meigen, 1818) s.l. Analyses of a variety of environmental factors recorded at the insects’ breeding sites showed that, by considering larvae and pupae together, the differences in the assemblages of blackfly species were explained by four variables: river depth, temperature, conductivity and elevation.
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Introduction: The effectiveness of Simuliidae (Diptera, Nematocera) as indicators of stream health was tested in the urbanizing area of Rome, Central Italy. Methods: 108 sampling sites were investigated in the spring to acquire data on environmental variables and black fly species. Results and discussion: The comparison of sampling and literature data highlighted the disappearance of some species (Simulium reptans, S. vernum, S. liriense), possibly due to water pollution and land use changes. Correspondence analysis confirms altitude as the main factor influencing black fly species' distribution. However, water quality becomes predominant when considering exclusively plain sites: "ornatum" and "equinum" species groups show the greatest tolerance to chemical pollution. The high course of the Aniene river and its tributaries were sampled bimonthly, confirming the spatial-temporal black fly successions previously observed in central Apennines. The results also indicate that S. ornatum may supplant all other species in areas where the rural use is substituted by urban landscape. Conclusion: In conclusion, black flies can be considered good environmental indicators to assess ecological health of both watercourses and surrounding landscapes.
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Water clarity in the Orange River of South Africa alternates between highly turbid and clearer conditions. Multiple ecological effects result from this that affect aquatic community structure and species composition, including switching of dominant black fly species and growth of benthic algae. Fourteen sites in the middle and lower Orange River were sampled for black fly species and abundances, presence of benthic algae, and water quality and turbidity seasonally between November 2015 and December 2016. Logistic regression models, time series analyses, and multivariate ordinations showed that clearer water favours benthic algae and the minor pest black fly species Simulium adersi Pomeroy, 1922 and Simulium nigritarse Coquillett, 1902, while high turbidity favours the major pest black fly species Simulium chutteri Lewis, 1965 and Simulium damnosum Theobald, 1903. Moreover, these switches appear to be less frequent under post-impoundment conditions. We conclude that black fly species composition is dynamic and reflects changes in flow and turbidity levels. Flow regulation has resulted in a trade-off between improved water supply and ecological costs resulting from reduced ecosystem variability.