INTRODUCTION

Hoverflies are diverse, both in species and ecology, and occur in most habitats and regions (Marshall, 2012), pollinate many plants and control populations of other insects (Rotheray & Gilbert, 2011). They can be used as indicators of habitat integrity (Speight & Castella, 2005) and Global Change (Rotheray & Gilbert, 2011). Changing climate may have negative effects on hoverflies; for instance, in southern Europe, populations of saproxylic species (larvae dependent on moist microhabitats in trees, such as rot holes) are thought to decrease in the future under a projected warming climate (Marcos García & Ricarte, 2009). Diversity comparisons over time in accordance with available climatic data may help to understand the effects of climate change on biodiversity, but this requires that temporal series of data on diversity surveys are available.

Highlands represent areas of endemicity and high biodiversity levels within the Mediterranean Basin (García-Barros et al., 2002; Reyero, 2002; Marcos-García et al., 2007). The Sierra de Guadarrama, located in central Spain, is one of the Iberian locations with the most significant biodiversity (Lobo et al., 2001; Lobo & Martín-Piera, 2002; Nieves-Aldrey et al., 2003). For example, 1310 species of Hymenoptera are known to occur at El Ventorrillo (Madrid), a representative site within Sierra de Guadarrama, and in total 13000 insect species are estimated to occur at this single site (Nieves-Aldrey et al., 2003). Its remarkable entomological diversity justifies the status of part of Sierra de Guadarrama as a national park since 2013. This Sierra is included mainly in the provinces of Madrid and Segovia, and most of the national park's surface belongs to the province of Madrid.

With 135 species, the province of Madrid has the third highest number of hoverfly species recorded for a Spanish province (Ricarte & Marcos-García, 2017; Grković et al., 2019; Van Steenis et al., 2020). Gil-Collado (1930) provided hoverfly records for 14 localities in the Sierra de Guadarrama: Cercedilla, Collado Mediano, El Escorial, El Espinar, El Paular, Guadarrama, Los Molinos, Lozoya, Navacerrada, La Granja/San Ildefonso, San Rafael, Sierra de Guadarrama, Valle del Paular and Valsaín (Fig. 1). Later on, Peris (1962) described Sericomyia hispanica Peris, 1962 based on specimens from Cercedilla and La Granja reported by Gil-Collado (1930) as Sericomyia lappona (Linnaeus, 1758). Marcos-García & Louis (2001) also reported some hoverfly species from Sierra de Guadarrama. Marcos-García et al. (2007) treated unpublished material of Merodon unguicornis Strobl in Czerny & Strobl, 1909 from Cercedilla and designated a lectotype for Merodon escorialensis Strobl in Czerny & Strobl, 1909 from two syntypes collected at El Escorial. Van Steenis & Lucas (2011) reported Pipizella lyneborgi Torp Pedersen, 1971 based on specimens collected at El Escorial 2-3 years after its original description.

Fig. 1.

Sierra de Guadarrama (Spain). El Ventorrillo is indicated with a red triangle. All labelled localities belong to Sierra de Guadarrama, although found outside the borders of the national park.

Within the Sierra de Guadarrama, some major insect groups are clearly understudied. For example, prior to this study only 27 species of five Dipteran families were known from El Ventorrillo (Kehlmaier, 2004, 2005; Kehlmaier et al., 2019), with no records of bioindicator families such as hoverflies. Between 1988 and 1991, insects were systematically surveyed at El Ventorrillo, with more than a million specimens caught. Diptera was the most abundant group in these samples, with nearly half of the total number of collected specimens (Nieves-Aldrey et al., 1991, 2003).

The main aim of the present study is to increase our knowledge on hoverfly distribution and phenology in the Sierra de Guadarrama by presenting a list of the hoverflies collected at El Ventorrillo with a Malaise trap over a one year period. The long term goal is to facilitate future comparisons of temporal diversities. The results are also placed in the wider framework of the hoverfly diversity of the Sierra de Guadarrama and that of the province of Madrid.

MATERIAL AND METHODS

Study area

The Sierra de Guadarrama, with altitudes above 2000 m, belongs to the Sistema Central mountain range of Spain. El Ventorrillo (40°45′16.5″N 4°01′15.5″W, 1482 m) is a Biological Station of the ‘Museo Nacional de Ciencias Naturales' (MNCN) (CSIC-Consejo Superior de Investigaciones Científicas), located on the south slope of Sierra de Guadarrama, in Cercedilla (Madrid province), about 60 km from the metropolis of Madrid (Nieves-Aldrey et al., 2003) (Fig. 1). The climate is subhumid Mediterranean tending to central European (Allué Andrade, 1987), with cold winters, possible freezes from September to June, 1000-1600 mm/year of precipitation, and a short, dry, and warm period in July-August (‘Puerto de Navacerrada’ as weather reference).

The area's vegetation is supra Mediterranean (Rivas Martínez, 1982), but the original vegetation has been largely replaced by plantations of Pinus sylvestris L. The vegetation at El Ventorrillo consists of a dense human-modified forest mainly of maples (Acer pseudoplatanus L.) and mountain elms (Ulmus sp.), but also linden, pine, cedar, fir, poplar, ash and holly. In the lower part of the Station, woodland is replaced by grasslands with roses and brambles. The vegetation at the forest/grassland edge consists of various shrubs such as Cytisus, Crataegus, Rubus, Rosa, Cistus, Santolina, Juniperus, and Prunus, while in close-by areas outside the Station some patches of Quercus pyrenaica Willd. with Cistus shrubs occur (Nieves-Aldrey et al., 2003) (Fig. 2).

Fig. 2.

El Ventorrillo in summer (Sierra de Guadarrama, Spain). Malaise trap placed in grassland/mix-forest edge.

RESULTS

Guilds, phenology, biogeography and conservation

In the Malaise trap samples, hoverflies of 51 species were collected, with 31 species of Syrphinae and 20 of Eristalinae (Table 1 and Appendix). Neither Microdontinae nor Pipizinae were collected. Zoophagous dominated both in species richness and abundance. In fact, a minimal proportion of individuals (below 3%) belonged to guilds other than zoophagous (Fig. 3).

Many species such as Cheilosia laticornis were recorded just from a short length of time within their flight period in Europe (Table 1). Callicera macquarti flies in June and September/October, but the female reported here was caught in early May. In a similar way, Callicera rufa is known to fly from mid May to August and the female recorded at El Ventorrilo was collected in early September. Didea intermedia was collected in September, one month after its flight period ends in Europe. For Merodon unicolor and Chrysotoxum volaticum, sub-populations from North Africa were also considered in the ‘European’ phenology. The phenology of Chrysotoxum intermedium is not provided since the taxonomy of this species is unresolved and several close taxa may exist under this name.

Fig. 3.

Guild diversity of El Ventorrillo hoverflies. Inner circle, for species richness; outer circle, for abundance. ‘Saproxylic’ is used for saprophagous species depending on trees.

Table 1.

Phenology of El Ventorrillo hoverflies. The flight period of adults in Europe is indicated with a black line while El Ventorrillo flight period is indicated in grey. Months: i, January; ii, February; iii, March; iv, April; v, May; vi, June; vii, July; viii, August; ix, September; x, October; xi, November; xii, December.

Continued

Most species collected at El Ventorrillo are typical for the Mediterranean zone of Europe (45 out of 51 spp.) closely followed by species occurring mainly in the Atlantic and Continental zones (40 spp. each). The lowest number of species are characterized having Macaronesian (16 spp.) and Arctic (12 spp.) distributions (Fig. 4). The majority of species recorded are unthreatened, four are decreasing in number of populations or range at the European level (Callicera rufa, Chrysotoxum cisalpinum, C. octomaculatum and Eumerus consimilis), and two are probably threatened with extinction (Callicera macquarti and Pelecocera caledonica). The latter two species were represented by singletons or doubletons in the sample. Chrysotoxum intermedium, C. latifasciatum, Merodon ibericus, and M. unguicornis are regarded as data deficient in Europe.

Fig. 4.

Biogeographic diversity of El Ventorrillo hoverflies. Species known to be present in each biogegraphic zone of Europe, expressed both in species richness (within grey bar) and percentage (above bar) calculated from the total number of species found at El Ventorrillo. Notice that a species can be present in more than one biogeographic zone.

Hoverfly fauna of Sierra de Guadarrama

With this study, 21 species are added to the checklist of the hoverflies of the Sierra de Guadarrama that is updated now to a total of 126 species (see Appendix). The genera Brachypalpus, Didea, Dasysyrphus, Neoascia, Parasyrphus, Syritta, and Xanthandrus are reported for the first time from Sierra de Guadarrama. Peris (1962) excluded S. lappona from the Spanish fauna of Sericomyia, but apparently he did not examine the material of S. lappona from El Escorial reported by Gil-Collado (1930). Thus, we retain S. lappona in the Sierra de Guadarrama checklist until this genus is revised in the Iberian Peninsula. The record of Chrysotoxum bicinctum (Linnaeus, 1758) from Cercedilla is likely to be a misidentification of C. volaticum but we retain C. bicintum in the Sierra de Guadarrama – and Madrid –checklist until the material from Cercedilla is revised. Although Syritta pipiens is one of the most common hoverflies in Spain (Gil-Collado, 1930; Ricarte & Marcos-García, 2017) and it is most likely to occur everywhere in Sierra de Guadarrama, the specimen reported here represents the first documented record from Sierra de Guadarrama. In the Malaise trap inventory discussed here, 40% of the species found in the Sierra de Guadarrama are represented.

Fig. 5.

Hoverfly diversity of Sierra de Guadarrama (species richness). All localities with hoverfly records in the literature are included. The category ‘undefined’ refers to unspecified localities within Sierra de Guadarrama. M, Madrid province; SG, Segovia province.

Within the Sierra de Guadarrama, El Escorial is the locality with the highest number of species recorded (64 spp.), followed by El Ventorrillo (51 spp.), both in Madrid province. Valle del Paular and Navacerrada, also in Madrid, are clearly under-recorded (one species each). La Granja/San Ildefonso is the Segovian locality in Sierra de Guadarrama with the highest number of species recorded, although the absolute number is still low (19 spp.) (Fig. 5). In 11 out of 14 localities of Sierra de Guadarrama, 50% or more of the collected species are eristalines, but the only locality sampled with a systematic technique, El Ventorrillo, has a higher proportion of syrphine species than eristaline species (61% vs. 39%). The hoverfly diversities in all the mentioned localities (Fig. 5) are not comparable with each other due to different sampling efforts and techniques used by the different collectors over time. However, Fig. 5 is still useful in understanding how uneven hoverfly knowledge is in Sierra de Guadarrama and to show basic tendencies based on Malaise trap sampling.

In this study, 17 species and two genera are new to Madrid province and the checklist of the Syrphidae from this province consists now of 150 species (Appendix). Madrid is still the third Spanish province in hoverfly species richness, after León (182 spp.) (Ricarte & Marcos-García, 2017) and Salamanca (152 spp.) (Ricarte et al., 2018). In the Malaise trap catch of El Ventorrillo, 34% of species found in the Madrid province are represented. Following the present study, microdontines are still uknown to the province of Madrid.

Fig. 6.

Hoverfly species from Sierra de Guadarrama. (A) Milesia crabroniformis, female, Puerto de Navacerrada. (B) Sericomyia hispanica, female, Puerto de Navacerrada. (C) Chrysotoxum sp. near vernale, male, Puerto de la Morcuera. (D) Dasysyrphus albostriatus, female. Photos A, B, D by Piluca Álvarez-Fidalgo, C by Marián Álvarez-Fidalgo.

DISCUSSION

In this study, 17 hoverfly species and two genera were found to be new to Madrid province from a Malaise trap catch originating from El Ventorrillo, Sierra de Guadarrama, dating from 1989-1990. One of the most remarkable aspects brought to light by these results is the lack of long term surveys of the hoverfly fauna of Madrid since 1989. Only a few species have been reported from Madrid in scattered publications in the last 30 years (see some examples in Appendix). On the one hand, these results show how important long term surveys are even in a province whose hoverfly diversity is thought to be well known (Ricarte & Marcos-García, 2017). On the other hand, the finding of 21 species new to Sierra de Guadarrama suggests the high potential of this location within the Iberian Peninsula for hoverfly diversity studies, as shown by other insect groups (Lobo & Martín-Piera, 2002; Nieves-Aldrey et al., 2003).

The hoverfly community of El Ventorrillo was represented in the Malaise trap catch by 51 species, most of them Mediterranean faunistic elements (Fig. 4), without records of Microdontinae and Pipizinae. Syrphinae were dominant in the samples, with more than half of the species (31 spp.) and individuals of Syrphidae identified (1999 out of 2050). These results were consistent with previous findings. For example, syrphines appear to be less specialised in flower visitation than other subfamilies (Klecka et al., 2018) and this fact is likely to facilitate a higher species diversity of syrphines with no regard of the plant community found in a study site. Syrphines are also known to be more diverse in forests than in other habitats (Branquart & Hemptinne, 2000). The Malaise trap used in the present study was placed in a grassland/ forest edge, so an influence from the forest community of syrphines was expected in the Malaise trap catch.

Sphaerophoria scripta and Eupeodes corollae, both of them syrphines, were the most abundant species in the sample, with 1146 and 351 specimens collected. These two species were not only abundant, but also occurred during a long period throughout the year, 5-6 months (Table 1). Sadeghi & Husseini (2009) also found in Iran that Malaise samples were clearly dominated by these two common species plus Episyrphus balteatus. The high ecological success of S. scripta and E. corollae is, without doubt, mediated by the high spectrum of prey of their zoophagous larvae, found in a wide range of plants, from herbs to trees (Rojo et al., 2003). In fact, zoophagous hoverflies dominate our Malaise trap sample from El Ventorrillo (Fig. 3).

Eristalines were more rarely collected than syrphines at El Ventorrillo, both in number of species and individuals. In addition, they had a shorter period of occurrence in the samples, of 1-2 months in most species (Table 1). This lower number of eristalines in the Malaise samples, with genera found in Sierra de Guadarrama poorly represented or even absent (see Appendix) is a consequence of the rarity and behaviour of some species. For example, Volucella hoverflies are frequently found flying high (Speight, 2020) and this behaviour reduces the chance for them to get captured with Malaise traps (just one specimen of Volucella in this Malaise catch). Saproxylic species such as those of Spilomyia are never abundant, their larvae live in tree rot-holes and adults visit flowers in grassy clearings (Speight, 2020). In a one-year long sampling with six Malaise traps in the woodlands of Cabañeros National Park (Ciudad Real) just two specimens of Spilomyia were collected (Ricarte, 2008). In general, Burgio & Sommaggio (2002, 2007) and Sommaggio & Burgio (2003) found that Malaise traps are less effective in catching saprophagous hoverflies (all saprophagous species are eristalines) than zoophagous (zoophagous species are syrphines, pipizines, microdontines, and a few Volucella species, which are eristalines).

Regarding the absence of Microdontinae and Pipizinae, we dismiss an overlook of these groups when sorting the Malaise catches because the person in charge was able to extract genera that can go unnoticed for someone with insufficient experience due to the small size and/ or uniformly dark colouration of these flies: Cheilosia, Eumerus, Neoascia, Paragus, Platycheirus, and Syritta. That said, no Microdon species has ever been collected in Madrid and adjacent provinces (Ricarte & Marcos García, 2017). This lack of information on Microdon from this part of Spain is most likely to be an artefact of the sampling techniques and collectors. Microdontines are rarely collected and their capture frequency with Malaise traps is low (Reemer, 2012). For example, two Microdon species occur in the Cévennes national park, France, but they were not collected in a two-year long study with two Malaise traps within the park (Descaves, 2016). The difficulty to catch microdontines with Malaise traps is likely due to the low mobility and behaviour of Microdon adults: some European species disperse just a few meters from their natal ant nests and, in addition, females appear to walk more than fly (Schönrogge et al., 2006; Wolton, 2011).

Pipizines is the other subfamily not represented in the Malaise catch of El Ventorrillo. Seven pipizine species are recorded from Madrid, five of them in Sierra de Guadarrama. However, records of all but one species are old (1930 or earlier) (Ricarte & Marcos-García, 2017); Pipizella lyneborgi Torp Pedersen, 1971, the exception, was recorded from a female collected in El Escorial in 1973 (Van Steenis & Lucas, 2011). The pipizine genus with the highest number of species recorded in Madrid is Pipizella Rondani, 1856 (see Appendix). The larvae of this genus are zoophagous in ant-attended aphids, but the larvae of most Pipizella species are unknown (Speight, 2020). Pipizines also appear to be rarely collected in Malaise traps. For example, in Cabañeros (Spain) no pipizine was collected with 10 Malaise traps in five different types of habitats during a year (Ricarte, 2008). In the Cévennes (France) just 1.4% of all collected hoverflies were pipizines (Pipiza + Pipizella) (Descaves, 2016). The absence of pipizines from the studied samples seem to be in accordance with the results of other Malaise-based surveys in Europe.

In this1989-1990 Malaise trap sample from El Ventorrillo, 41% of the species known from Sierra de Guadarrama were collected. In the Cévennes national park's sampling effort mentioned above, one trap/year collected an average of 39% of the species recorded from this national park (Descaves, 2016), which is a very similar proportion as that between El Ventorrillo and Sierra de Guadarrama. In addition, the Malaise traps used both in the Cévennes and El Ventorrillo failed in catching microdontines and had a low success in catching pipizines (none in El Ventorrillo), as explained above. From this and other studies (e.g. Sommaggio & Burgio, 2003; Ricarte, 2008; Descaves, 2016), it is obvious that Malaise traps do not provide a full inventory of species found in an area. However, the hoverflies of a Malaise trap catch represent the community of at least the two major subfamilies (Eristalinae and Syrphinae) and provide the means to compare the largest proportion of the hoverfly diversity of a site through time, as Malaise traps, if set up at the right location, allow a systematic sampling of easy repetition with no regard to the collector skills and experience. Thus, although for a full species inventory of an area different sampling techniques should be used (Ricarte, 2008; Marcos García et al., 2012), Malaise traps provide an adequate experimental design and baseline to compare tendencies in the hoverfly diversity over time. We consider that the species sample presented here could be compared with future samples obtained from El Ventorrillo with a similar sampling design.

With 126 species, Sierra de Guadarrama has 83% of the species recorded from Madrid province, and this becomes the most diverse location of Madrid and adjacent provinces for hoverflies. This high hoverfly diversity is in accordance with the high levels of biodiversity reported for other insect groups in Sierra de Guadarrama (e.g., Lobo & Martín-Piera, 2002; Nieves-Aldrey et al., 2003). However, the proximity of Madrid city has surely had an effect in the knowledge of biodiversity in Sierra de Guadarrama, because many collectors from the city have focused on this location for fieldwork along history; for example, collectors used to sample hoverflies in localities within Sierra de Guadarrama at least since the early twentieth century (Gil-Collado, 1930). Even nowadays, Sierra de Guadarrama is the preferred and most convenient area for city naturalists to monitor biodiversity (Fig. 6). This long history of surveys and monitoring together with the set of data provided here for El Ventorrillo makes Sierra de Guadarrama suitable for planning studies on the effects of Global change on the biodiversity of Syrphidae.

El Ventorrillo is a shelter for species of hoverflies with decreasing populations in Europe or even threatened with extinction. Callicera macquarti (‘threatened') belongs to the saproxylic guild, with larvae developing in rot holes of mature trees (Ricarte et al., 2009). Thus, forestry practices at El Ventorrillo and surroundings should allow trees to grow in size and develop holes, to promote the breeding of this rare species distributed around the Mediterranean. Pelecocera caledonica (‘threatened') is present from Scandinavia and European Russia to Spain, where it was known only from Navarra (Speight, 2020). To propose conservation actions for P. caledonica would be more difficult than for C. macquarti since its larval biology, although suspected to be phytophagous, is completely unknown; further research on the larval biology of P. caledonica is required. El Ventorrillo populations of these two species and those of the ‘decreasing’, C. rufa, C. cisalpinum, C. octomaculatum, and E. consimilis, should be monitored to better understand the population size and trend in this part of Europe.