(Diptera) Larvae: a Brief Review and a Key to European Families Avoiding Use of Mouthpart Characters

1 Article

Family-level keys to freshwater fly (Diptera) larvae: a brief review and a key to European families avoiding use of mouthpart characters

Michael Dobson1 1 Affiliation: Freshwater Biological Association, The Ferry Landing, Far Sawrey, Ambleside, Cumbria, LA22 0LP, UK.*

*Present address: APEM Ltd, The Technopole Centre, Edinburgh Technopole, Milton Bridge, Nr Penicuik, Midlothian, EH26 0PJ, UK. Email: [email protected]

Received 3 October 2011; accepted 10 April 2013; published 18 June 2013

Abstract

Identification of larvae of aquatic Diptera (true flies) is complicated by a range of factors, including reliance on examination of mouthparts at the very beginning of many keys, as well as an unclear distinction between aquatic and terrestrial habits for many species. Even at family level, these can cause problems. This review briefly introduces the history of keys to Diptera larvae, with particular reference to Europe, and identifies use of characteristics that may cause problems for the non-specialist, along with attempts made to mitigate these problems. It considers the validity of using identification features that do not require examination of mouthparts, giving examples of those used in previous keys. It then reviews Diptera families that are not normally considered to have aquatic representatives, concluding that in Europe six new families need to be added to the list of freshwater fauna: Cecidomyiidae (rivers and tree holes), Scatopsidae (tree holes), Anisopodidae (tree holes), Bibionidae (probably wetlands), Pachyneuridae (saturated dead wood) and Lonchopteridae (river edges). Elsewhere in the world, a further nine families have been recorded from fresh waters, all from submerged dead wood or from water-filled plant structures such as pitcher plants and tree holes. A dichotomous key to European families of aquatic Diptera is included, based purely on external morphology without reference to mouthparts, and incorporating the six families highlighted above. This key is copiously illustrated with line drawings, mainly of whole animals.

Keywords: Aquatic Diptera larvae; diagnostic key; dichotomous key; external morphology; macroinvertebrate identification; synoptic keys.

Introduction Diptera (true fly) larvae are by far the most diverse group, and the ones encountered in the widest variety Among the macroinvertebrates found in fresh waters, of habitats, from large lakes to tree holes and temporary

DOI: 10.1608/FRJ-6.1.450 Freshwater Reviews (2013) 6, pp.1-32 © Freshwater Biological Association 2013 2 Dobson, M. pools, plus all types of running waters. Unfortunately, head so that it becomes much less obviously recognisable for the non-specialist they can also cause some of the as such. biggest difficulties in identification. For a few families The first group, the Nematocera, contains those families and geographical regions there are comprehensive keys to whose larvae have a fully developed head capsule, with species (e.g. Bass, 1998; Disney, 1999), but for most, keys mandibles that move opposably (in a horizontal plane, are out of date, incomplete or even simply absent. pincer-like – see Fig. 1a); most of its families have an affixed Furthermore, definitive identification even at the head but the Tipuloidea (containing the families Tipulidae, level of family can be problematic. The systematic Limoniidae, Pediciidae and Cylindrotomidae) are able to characteristics used to differentiate key groupings within retract their heads into the thorax. A clear exception to the the order, and therefore to produce a taxonomically general structure is the family Cecidomyiidae, whose head accurate key, require examination of the morphology of the heads, and particularly the mouthparts, which a) may not be possible without dissection. Probably the majority of people having to identify freshwater Diptera are those working for statutory water agencies in routine monitoring, and considerable experience by the author in providing identification training for such organisations has demonstrated that distinguishing different mouthpart types is a consistent issue, as few of their staff have the appropriate knowledge or experience of dissection techniques. Additionally, relatively few students embarking on ecological studies have such training, jeopardising effective identification and recording of aquatic Diptera. This review attempts to address this issue by developing an alternative method for identifying freshwater Diptera b) larvae. It initially considers the morphological problems encountered when producing a simple key to aquatic Diptera families, and then briefly reviews the families that occur in fresh waters, with particular reference to those that are not normally considered to be part of the aquatic fauna. Finally, it presents a key to European freshwater Diptera families, avoiding the morphological features that cause the non-specialist so much trouble when using most of the currently available keys to the group.

Features of taxonomic importance in identifying larval Diptera

The order Diptera is divisible into three groups, based on structure of the head and mouthparts. These represent an Fig. 1. (a) Pediciidae, dorsal view, highlighting opposing mandibles (m) of Nematocera, paired posterior respiratory evolutionary trend across the group of loss of sclerotisation spiracles (sp) and prolegs (pr); (b) Tabanidae: head and front of (hardening) of the head capsule, and modification of the thorax, ventral view, showing parallel mandibles of Brachycera.

© Freshwater Biological Association 2013 DOI: 10.1608/FRJ-6.1.450 Family-level keys to Diptera larvae 3 capsule and mandibles are vestigial. The second group, Approaches used by keys to the Brachycera, contains families whose head capsule is freshwater Diptera families reduced but still clearly identifiable as such, along with mandibles that are parallel, and operate in a vertical Identification keys come in two basic types. Synoptic keys plane (Fig. 1b); almost all have heads that are retractable are those which distinguish taxa on the basis of characters into the body cavity, although there is one exception, that reflect evolutionary relationships and are therefore the Stratiomyidae. The third group is the Cyclorrhapha, used in taxonomic classification. Diagnostic keys use also with mandibles that are parallel, but in which artificial distinctions: those that are more straightforward the head capsule is so reduced as not to be obviously to identify, even if they have no role in determining identifiable as such. An important differentiation between evolutionary relationships. The advantage of synoptic Brachycera and Cyclorrhapha, albeit one that requires keys is that the features they use are definitive, but while high magnification and dissection, is the structure of they may be obvious they may equally be obscure or the pharyngeal skeleton, sclerotised rods that project difficult to see. Diagnostic keys are designed tobeas from the head into the body; among Cyclorrhapha the easy as possible, but can be confusing when a specimen is branches are fused towards the front (Fig. 2), whereas among Brachycera they can move relative to each other. a) In practice, however, if you are dissecting a brachyceran, an identifiable head capsule, usually with obvious eye spots, will tell you that it belongs to this group, and further dissection to find the pharyngeal skeleton is not necessary. These divisions are based on the larval characters that were used by Brauer (1883), who first classified Diptera into suborders. His original classification saw the Cyclorrhapha as a suborder, while the Nematocera and Brachycera were divisions of a second suborder, the Orthorrhapha. The two names derive from a further differentiation identified by Brauer: the mechanism by which the emerging adult escapes from its pupal skin. Adults of Cyclorrhapha (meaning ‘circular seamed’) escape from a semi-circular aperture, while those of Orthorrhapha (‘straight b) seamed’) escape from a T-shaped aperture. Modern classifications continue to use these names, but have altered their relationships somewhat, with the Nematocera considered a suborder, while the Cyclorrhapha and Orthorrhapha are generally considered to be subdivisions within a second suborder, the Brachycera (Table 1).

Fig. 2. Pharyngeal skeleton of Limnophora (Muscidae): (a) head and thorax, with the pharyngeal skeleton visible as a dark feature within the thorax; it is rarely this obvious without dissection; (b) the pharyngeal skeleton partially dissected; the length of this structure is approx. 1 mm.

DOI: 10.1608/FRJ-6.1.450 Freshwater Reviews (2013) 6, pp. 1-32 4 Dobson, M.

Table 1. Diptera families normally considered to have aquatic representatives. Families in bold occur in Europe.

a) Nematocera Blephariceridae Exclusively aquatic Ceratopogonidae Peripherally aquatic Chaoboridae Exclusively aquatic Chironomidae Mostly aquatic Culicidae Exclusively aquatic Deuterophlebiidae Exclusively aquatic Dixidae Exclusively aquatic Nymphomyiidae Exclusively aquatic Psychodidae Peripherally aquatic Ptychopteridae Exclusively aquatic Simuliidae Exclusively aquatic Tanyderidae Exclusively aquatic Tipuloidea Cylindrotomidae Terrestrial and aquatic Limoniidae Mostly terrestrial; some peripherally aquatic Pediciidae Mostly aquatic Tipulidae Mostly terrestrial; some aquatic Thaumaleidae Exclusively aquatic

b) Brachycera – “Orthorrhapha” Athericidae Mostly terrestrial; some aquatic Empididae Mostly aquatic or peripherally aquatic Rhagionidae Mostly terrestrial; some peripherally aquatic Stratiomyidae Mostly terrestrial; some aquatic Tabanidae Mostly peripherally aquatic; some terrestrial

c) Brachycera – “Cyclorrhapha” Dolichopodidae Mostly aquatic Ephydridae Mostly aquatic Muscidae Mostly terrestrial; some aquatic Scathophagidae Mostly terrestrial; some peripherally aquatic Sciomyzidae Terrestrial and aquatic Syrphidae Mostly terrestrial; some aquatic encountered that does not follow the diagnostic features following Brauer (1883), required an initial determination exactly. of orientation of mandibles, followed by, for those moving Among Diptera larvae, a synoptic key would start in a vertical plane, the structure of the pharyngeal skeleton. with the subdivisions described above, and indeed this is Hennig (1948, 1950, 1952), in many ways the definitive the format followed by the earliest keys. Malloch (1917), account of dipteran larval morphology, also followed this

© Freshwater Biological Association 2013 DOI: 10.1608/FRJ-6.1.450 Family-level keys to Diptera larvae 5 division, as did Brindle & Smith (1978), whose key was obvious morphological characteristics, before ending later expanded by Smith (1989). Borkent & Rotheray (2009) with a descriptive approach to identifying the Brachycera followed this approach, with the useful exception of first and Cyclorrhapha. Macan was influenced by Bertrand separating the aberrant nematoceran family Cecidomyiidae (1954) and, although he did not state it explicitly, he (see later for discussion of the aquatic status of this family). made a primary separation using the presence or Keys specific to freshwater families are able to exclude otherwise of a hardened, non-retractable head capsule many families and therefore to be a little simpler. Johannsen (although he felt unable to include the Stratiomyidae in (1934, 1935) followed the synoptic approach of Malloch the fixed-head grouping). Fitter & Manuel (1986) settled (1917). However, the first modern key to freshwater on a descriptive approach, although they included a Diptera larvae in Europe, that of Bertrand (1954), was short key to main groupings that reverted to the synoptic slightly different in that it used as its primary character, approach, referring to mouthparts from the beginning. in addition to the orientation the mandibles, the state of Tachet et al. (1980) had produced the first version of development of the head capsule. Thus the Nematocera what was to become an excellent pictorial key (Tachet et were identified as having a well-developed head capsule al., 2000; most recent edition: Tachet et al., 2010). Their along with horizontal mandibles, the Orthorrhapha by approach was to use the presence or otherwise of a fixed having a fairly well developed head capsule (“assez head capsule as the primary division, following which bien développée”) and the Cyclorrhapha by having a those with a clearly visible external head (most Nematocera, reduced head capsule. The second division determined along with Stratiomyidae) subdivide into families using whether the head was fixed or retractable. Although normally quite distinctive characteristics. Sundermann Bertrand (1954) expected examination of mouthparts, et al. (2007) adopted the same approach, which was also this appreciation of the value of the general structure followed by Oscoz et al. (2011) and Dobson et al. (2012). of head capsule, along with whether the head is fixed The problem arises once the families with fixed and visible externally, was an important development. external head capsules have been covered. Here, it is However, it still required formal division into suborders useful to cover the Tipuloidea before the rest. However, before the two non-typical groups – Tipuloidea and they are very variable and the only common feature Stratiomyidae – could be considered (and he did not that separates them from the remaining families is the consider Cecidomyiidae at all). The same approach presence of horizontally-moving mandibles. Therefore, was followed by Smith (1997), the first comprehensive even the ‘user-friendly’ diagnostic keys of Sundermann key in English to freshwater Diptera families in Europe. et al. (2007), Tachet et al. (2010), Oscoz et al. (2011) and The problem for the general user is the technical Dobson et al. (2012) require examination of mandibles. difficulty of starting a key with mouthpart morphology; Sundermann et al. (2007) separated the Syrphidae and not only are the mouthparts often difficult to see but Ephydridae before dealing with the mouthparts issue, there are some apparent exceptions in each group and, in using a single posterior extension as the key feature, but one family, the Syrphidae, the mandibles are so reduced unfortunately these two families are variable in form to as not to be identifiable to any of the groupings. The the extent that this feature will not work consistently. issue of mouthparts has therefore provided problems Following division from Tipuloidea, the remaining for both creators and users of keys to larval Diptera. families are most easily determined in a diagnostic Macan (1959) created a key to freshwater invertebrates key using non-systematic external features, so that, that was specifically aimed at the non-specialist user. unlike Smith (1989, 1997) there will be no initial He appreciated this problem of relying on mouthpart separation of Cyclorrhapha from the remainder of morphology and avoided it completely by picking off Brachycera. In most cases, these features are clear, families within the Nematocera individually using but there are several families in which morphology is

DOI: 10.1608/FRJ-6.1.450 Freshwater Reviews (2013) 6, pp. 1-32 6 Dobson, M. highly variable, albeit with a ‘typical’ morphology that spiracles altogether. Fortunately, the other families the freshwater biologist is most likely to come across if in this grouping are more homogeneous and can be confining collection to rivers or lakes and not looking separated from each other with relatively little difficulty. in unusual habitats; this is considered further below. Another feature of some value is that of general body shape, used by Gooderham & Tsyrlin (2002) to differentiate Other characters of value to identification a group of families with long, parallel sided bodies from a group with bodies that taper towards the front. It is, A user-friendly key would rely on external characteristics however, not diagnostic and, as Fig. 3 shows, can be difficult that are relatively easy to identify. Fortunately, there is a to interpret, so can only be used as a supplementary feature. wide variety of such features among Diptera larvae, some Problems arise when the features described are not of which are currently used in their classification and obvious. The Syrphidae, Ephydridae and Muscidae each therefore synoptic characters; others are of little value in include a ‘typical’, commonly encountered form, plus classification, and therefore artificial diagnostic characters. various other, more rarely seen morphological types. Respiratory spiracles (Figs 1a, 6c) are valuable Among the Syrphidae, the classic ‘rat-tailed maggot’ is identification features. These are the apertures by which very distinctive with its blunt-ended body and single long oxygen is taken into the body. Diptera larvae may have two telescopic tail (Fig. 4a); other members of the family are, pairs, one towards the front of the thorax and one at the rear however, less obvious, the most extreme being the genus of the abdomen, a condition described as amphipneustic Melanogaster, whose single respiratory tube is reduced (amphi- on both sides; pneustic – referring to breathing); a single pair at the rear, referred to as metapneustic (meta- a) towards the rear); or in a series of pairs along the body segments, a state known as peripneustic (peri- around). There are also some larvae that are apneustic, lacking spiracles entirely (a- absent). Most of the aquatic Diptera with retractable or vestigial head capsules have paired posterior spiracles and these spiracles and their associated body architecture often follow consistent patterns. Among some families the spiracles are on the end of extensions, which are clearly separate (Ephydridae, Muscidae) or fused together (Syrphidae). In others, the spiracles sit flush with the end of the abdominal segment in a spiracular disc b) (e.g. Figs 6c, 27), surrounded by various appendages (e.g. Tipulidae, Limoniidae, Rhagionidae, Dolichopodidae, Sciomyzidae, Scathophagidae). The morphology of the spiracular disc allows further separation of those families that possess this feature, as several families have distinct and unique arrangements of lobes around the disc. Here, the disadvantages of using artificial characteristics come to light because one family, the Limoniidae, shows considerable variation, Fig. 3. Examples of Diptera larvae without a fixed external head capsule, showing how the body often tapers towards the head, variously having four or five appendages, no appendages which is to the left in these examples (contrast with Fig. 4): (a) and no obvious spiracular disc and, in one genus, lacking Tabanidae (genus Chrysops); (b) Muscidae (genus Limnophora).

Fig. 4. Examples of Syrphidae, showing the truncate front end, which is to the left in these examples (contrast with Fig. 3), and the variety of different respiratory structures (arrowed): (a)Helophilus , a rat-tailed maggot, with a telescopic siphon comprising a single elongated feature; (b) Melanogaster, with a siphon adapted as a short piercing spine; (c) Platycheirus, a terrestrial genus, showing the two spiracles clearly fused but also easily identifiable as two structures. in size to a small highly specialised piercing needle two ends are adapted into piercing needles, the single basal (Fig. 4b). The situation is more difficult among terrestrial section is no longer visible. These therefore can be easily members of this group (which occasionally occur by confused with Muscidae, another variable group whose accident in freshwater samples). All Syrphidae have two most commonly encountered genus, Limnophora, is very spiracles, as close examination of the end of the tail of a distinct (Fig. 3b) but whose other aquatic genera less so. rat-tailed maggot will reveal, but in the aquatic forms A user-friendly key has four options when dealing the appendages are so closely fused as to appear to be a with these non-typical forms. The first, adopted by single structure. In contrast, among terrestrial species Sundermann et al., (2007), is to specify that their key is there are clearly two appendages, albeit fused along the designed for Diptera found in a restricted range of habitats, central line (Fig.4c). Ephydridae are characterised by in their case rivers, and therefore to overlook the ‘difficult’ the very distinctive Ephydra and Setacera, with their large taxa not normally occurring in this habitat. The second, prolegs and distinctive respiratory siphon (Fig. 25a), but adopted by Tachet et al. (2010) and Oscoz et al. (2011), is the family is very diverse, even within aquatic forms. A simply to omit them without comment. The third, adopted defining feature is that there is a single siphon that divides, by Dobson et al. (2012), is to include an appropriate division but among the genera Hydrellia and Notophila, in which the into families, and then to continue to a more precise level

DOI: 10.1608/FRJ-6.1.450 Freshwater Reviews (2013) 6, pp. 1-32 8 Dobson, M. of within-family identification. The fourth, adopted Table 2. Other families with aquatic representatives. Families in bold have been recorded from fresh waters in Europe. All are here, is to consider each alternative form as a taxonomic mainly terrestrial. See text for more details. unit that may justify its own end point in the key. a) Nematocera Families with aquatic Anisopodidae representatives Axymyiidae Bibionidae Determining whether a dipteran family has aquatic Cecidomyiidae representatives can be confounded by the definition used Mycetophilidae for an aquatic environment. The damp soil at the edge of Pachyneuridae water bodies requires its inhabitants to be physiologically Scatopsidae adapted to a water-dominated environment, and Sciaridae individuals may therefore occasionally end up in the adjacent truly aquatic environment with no ill effects, b) Brachycera – Orthorrhapha but this does not necessarily make them aquatic. Many Pelecorhynchidae Diptera larvae are adapted to living in such specialised Xylophagidae waterlogged environments, including fresh dung and rotting corpses as well as mud. Species that are adapted to c) Brachycera – Cyclorrhapha living in wet rotting wood will not necessarily differentiate Calliphoridae between rotting wood in wet soil and rotting wood under Lonchopteridae water. In addition, many Diptera species are entirely Phoridae unknown in the larval form, so their preferred larval Sarcophagidae habitat is also unknown. Tachinidae For these reasons, the definition of what is an aquatic family has to be flexible. Table 1 gives a list of families widely from water contained within fallen leaves of the nikau accepted as having aquatic representatives. Most are palm (Rhopalostylis sapida H. Wendl & Drude) in New global in distribution, only three being absent from Europe Zealand (Derraik & Heath, 2005). Scatopsidae are and among the European families only Blephariceridae specialists on dung and dead wood, and Johannsen (1934) are restricted, being confined to southern and central recorded a case of specimens appearing under bark in parts of the continent. This list excludes the Canaceidae, floating spruce logs in the USA. Since then, the family has which is confined to the marine intertidal (Smith, 1989). been recorded from wet tree hole debris in England (e.g. In addition to those families listed in Table 1, there Laurence, 1953), from a truly aquatic tree hole environment are various others that have been recorded as having in France (Haenni & Vaillant, 1994; Wagner et al., 2008), aquatic or semi-aquatic representatives, six of these in and from water-filled bamboo nodes in Peru (Louton et Europe (Table 2). Tree holes are frequented by specialist al., 1996). Wagner et al. (2008) list Bibionidae as having members of families that are established as having aquatic been found in aquatic environments, although without representatives, particularly Chironomidae, Culicidae providing further details. This family is occasionally and Syrphidae. In addition, however, more unusual encountered in samples from streams (J. Pretty, personal families occasionally turn up. Kitching (1969) recorded a communication), and is normally assumed to be an temporary occupation by Sylvicola (=Anisopus) fenestralis accidental, but its presence in fresh waters needs closer (Scopoli), a member of the family Anisopodidae in investigation; Bibio rufipes (Zetterstedt) certainly seems Wytham Woods, England; this genus was also recorded to prefer wet habitats (Skartveit 2002). Pachyneuridae

© Freshwater Biological Association 2013 DOI: 10.1608/FRJ-6.1.450 Family-level keys to Diptera larvae 9 is represented in Europe by a single species – Pachyneura are external parasites of other insects, and some fasciata Zetterstedt – which is confined to Sweden and have aquatic hosts, the parasite deriving its oxygen Finland, and doubtfully Italy (Fauna Europaea, 2013). It from its host’s tracheal system (Johannsen, 1935). develops in decaying wood, is probably semi-aquatic and The water contained within pitcher plants and was recorded from wetland habitats by Salmela et al. (2007). bromeliads supports a diverse dipteran fauna. For example, Exposed sediments along the edges of rivers pitcher plants of the genus Nepenthes in south east Asia support many dipteran families including, in addition typically contain members of widely recognised aquatic to truly aquatic families, Therevidae, Asilidae, families, but in addition there may be representatives of the Hybotidae, Lonchopteridae, Phoridae, Micropezidae, families Calliphoridae, Cecidomyiidae, Mycetophilidae, Sphaeroceridae and Anthomyiidae (Godfrey, 1999). Phoridae, Sarcophagidae and Sciaridae (Mogi & Yong, All would have to be adapted to withstand occasional 1992; Mogi & Chan, 1996); Cecidomyiidae, Phoridae and inundations, but Vaillant (2002) describes two species Sciaridae were also recorded from flooded bamboo nodes in of Lonchoptera (Lonchopteridae) as being truly aquatic. Sulawesi by Sota & Mogi (1996). Several species of Phoridae The sixth family, Cecidomyiidae, comprises many specialise in pitcher plant and bamboo node habitats, gall-making insects as larvae, but also a wide variety particularly in south east Asia (e.g. Disney, 1991, 1995), but of free-living forms. Johannsen (1934) conceded that also in the Americas (Disney et al., 2009). North American some are occasionally found in submerged galls, but pitcher plants (genus Sarracenia) support members of the considered that, as they have no specific adaptation Sarcophagidae (Fish & Hall, 1978; Dahlem & Naczi, 2006), for living in water, they cannot be considered truly clearly adapted for an aquatic lifestyle, having a posterior aquatic. However, Thomas (1980) described a species structure to protect the spiracles of this air-breathing from the French Pyrenees whose larvae are free-living in species and to provide buoyancy (Johannsen, 1934). submerged mosses in torrential streams, while Churchel & Batzer (2006) listed this family as numerically oneof Notes on the key to freshwater the most abundant in streams in Georgia, USA. Several Diptera larvae free-living specimens have recently been taken in debris towards the edge of a river in Belize (R. Carrie, personal The key presented here has two aims: (1) to provide a communication), so the aquatic status of this family is clear. means for identifying aquatic Diptera larvae to family Elsewhere in the world, more families have been level without the need to examine mouthparts; (2) to recorded from fresh waters. The majority of these are incorporate the ‘new’ aquatic families into a key to aquatic also found in Europe but have not, so far, been found in Diptera larvae. aquatic habitats there. In the USA, Dudley & Anderson This key is purely diagnostic in that it does not use (1982) recorded several families in submerged and systematic characteristics to differentiate groups, except partially-submerged dead wood in streams: Axymyiidae where these are also user-friendly, and that it relies heavily (Axymyia sp., whose aquatic life history is described in on superficial characters that are of little taxonomic Wihlm & Courtney, 2011); Xylophagidae (Xylophagus); significance. It is also a first attempt at such an approach, Mycetophilidae (Symemerus and other unidentified and will no doubt require improvements in due course. genera); Pelecorhynchidae (Glutops); and Pachyneuridae The terminology used is as simple as possible, without (Cramptonomyia spenceri Alexander). As dead wood is being ambiguous. In a strict zoological sense what are here poorly investigated in fresh waters, it is possible that more referred to a ‘hairs’ should be called ‘setae’, but the term wood-boring families will turn up in Europe in due course. ‘hair’ has a general meaning that is widely understood, Johannsen (1935) refers to two species of Tachinidae so is preferred here. The terms proleg and welt are used. associated with fresh waters in North America. These Prolegs are fleshy leg-like appendages Figs( 1a, 5a), often

DOI: 10.1608/FRJ-6.1.450 Freshwater Reviews (2013) 6, pp. 1-32 10 Dobson, M.

a) b)

Fig. 5. (a) Atherix (Athericidae), highlighting one of the ventral prolegs (pr); (b) Antocha (Limoniidae), highlighting examples of dorsal (dw) and ventral (vw) welts, along with the anal papillae (ap). alternatively referred to as pseudopods, which an animal between protrusions from the main body and true uses for locomotion; often, but not always, prolegs have prolegs. Therefore, several families key out at two hooks or spines on their base and they are always found end points so that different interpretations of the same only on the ventral side. Welts are structures, also used feature should not result in an incorrect diagnosis. in locomotion, that are normally more flattened against No attempt is made here to provide keys that go the abdomen, are hardened and pigmented pads, and beyond family level, except where this is required to are not always confined to the ventral side (e.g. Fig. 5b). determine the family. Where a family has multiple end Of the families listed in Table 2, only those that have been points in the key, a specific genus is named only if itis recorded in European fresh waters are included. Of these unmistakeable as such. For further identification, the families, five - Anisopodidae, Bibionidae, Cecidomyiidae, reader is referred, for basic subdivisions and distinctive Lonchopteridae and Scatopsidae - have been included species, to Dobson et al. (2012), which covers Diptera from using reference to terrestrial specimens, information in all water bodies and also provides lists of more detailed Smith (1989) and, in the case of Cecidomyiidae, aquatic keys for much of the British fauna; and to Sundermann specimens from outside Europe; information about et al. (2007), which mainly covers rivers. As with any Pachyneuridae has been derived from Fitzgerald (2005). group of organisms, skills at identification are developed Meillon & Werth (2003) provide useful information by examining as many different specimens as possible. for including the Leptoconopinae (Ceratopogonidae), Identification is a technical process, requiring training and a subfamily which I have not seen. Anisopodidae ongoing development of experience. While identification and Pachyneuridae are not included as end points in keys are essential for developing this understanding, themselves; each has been recorded from fresh waters very there is no substitute for accessing a collection of rarely, but they are highlighted at points where they may named, preserved specimens. Museums often hold be confused with other families. Further families may turn such collections and, once confident identifications up, particularly those associated with submerged rotting have been made, addition to a personal or laboratory wood. Therefore, it is recommended that if this, or any reference collection creates a valuable ongoing resource. other non-typical habitat, is sampled, then identification should proceed with caution and, if in any doubt about the family caught, expert advice should be sought. Limoniidae – a special case Several families will key out at several different end points, representing morphologically different In writing a diagnostic key to Diptera, one family causes types. Furthermore, the key acknowledges that some particular difficulty because of the morphological features may be difficult to interpret for users with variability that it shows. Unlike the Ceratopogonidae, little experience, particularly relating to the difference another very variable family, the different morphological

© Freshwater Biological Association 2013 DOI: 10.1608/FRJ-6.1.450 Family-level keys to Diptera larvae 11 types of Limoniidae do not correspond to subfamily Antocha have a pair of spiracles, but the architecture of the divisions. Structurally, limoniids are superficially spiracular disc around these can include four long lobes, similar, with an extended cylindrical body showing two long and two short lobes, five lobes, four lobes that relatively few obvious features for most of its length (as in have closed up so they create a conical structure, no lobes Figs 6a, 34c), although some have dorsal and ventral welts but a clear spiracular disc, or no lobes and no apparent (Figs 5b, 6c), some have ventral welts only (Fig. 6d) and spiracular disc (see Figs 6, 27, 34). Some have very distinctive others (the majority) have no welts at all. Many are covered tufts of long hairs (Fig. 6b), which are diagnostic for some in fine hairs, giving the animal a downy appearance, and members of this family but only found on certain genera. this can be very marked in darker mature specimens; Finally, many members of this family will inflate however, a few are smooth and lacking in such hairs. the rear abdominal segment, as shown in Fig. 6a. The main location of morphological variation in Again, this is diagnostic for this family, but is not this family is the rear of the abdomen. All but the genus

a) b)

Fig. 6. Examples of Limoniidae: (a) Eloeophila, highlighting the inflated rear segment often seen in Limoniidae; (b) Pseudolimnophila, highlighting tufts of long hairs (h), spiracular lobes (sl) and large anal papillae (ap); (c) Dicranomyia, highlighting the pale dorsal (dw) and ventral (vw) welts and the prominent spiracles (sp) within a spiracular disc lacking lobes; (d) Helius, highlighting a ventral welt (vw).

DOI: 10.1608/FRJ-6.1.450 Freshwater Reviews (2013) 6, pp. 1-32 12 Dobson, M. consistent, so within the same species there may be rear end of the abdomen (Figs 5b, 6b, 33b) and can specimens with and others without this inflation. sometimes be very long. 2. Families with a retractable but otherwise clearly Words of caution in using this key identifiable head capsule (Tipuloidea, Tabanidae, Rhagionidae, Athericidae) may, in preserved samples, A key such as this requires an understanding of several occasionally have died with their head exposed. This important points. is particularly the case for larvae killed by immersion 1. For families without a fixed external head capsule, the in boiling water, an example of which is illustrated in spiracular disc and its structure is used extensively as Fig. 3a. Therefore, make sure that an exposed head a diagnostic feature. If asked to look for lobes, make is truly a fixed head capsule and not one that could sure that you are looking at the structures around otherwise have been withdrawn. A retractable head the spiracular disc itself, and not anal papillae, which will be clearly narrower than the first segment of the are commonly encountered on the ventral side of the thorax, and the base of the head will extend into the fleshy part of the body.

Key to families of freshwater Diptera larvae in Europe

The key is dichotomous throughout. At each point, choose one of the options and then proceed to the number given until you reach an end point. Where a couplet is reached from a point other than the previous couplet, the number of the couplet from which you have come is also given in parentheses. The author welcomes any comments on this key, particularly those relating to points where it does not work well, improvements that could be made and particular specimens that cannot be keyed out. Note that all line drawings of whole animals show them in lateral view, unless otherwise stated, and the head is always to the left. Note also that the illustrations are not to scale; the text at the end points in the key give an indication of the approximate maximum size of the different families.

1. Distinct head capsule present, not retractable into the soft body (the head may be very small) 2

₋₋ No obvious head capsule, or head retractable into soft body 17

Fig. 7. Blephariceridae, ventral view.

2. Body with six apparent segments, each with a distinctive ventral sucker Blephariceridae (Fig. 7) Up to 10 mm long. Central and southern Europe only. Each body segment is constricted front and rear, giving an unmistakeable body shape. Fast-flowing parts of torrential streams.

₋₋ Body clearly with more than six segments, or segmentation unclear; no ventral suckers 3

3. Each body segment with distinct lateral (and often dorsal) extensions 4

₋₋ Extensions absent or confined to the rear end of the abdomen 5

4. Prolegs absent; a line of darkened oval spiracles present along each side of the body, along with a distinct pair of larger spiracles towards the rear Bibionidae (Fig. 8a) Up to 15 mm long. Body cylindrical, with rows of short soft extensions. Rarely encountered in water, but found in wet marshes and also occasionally recorded in streams.

₋₋ Prolegs present on the first segment of the thorax; spiracles not obvious Ceratopogonidae: subfamily Forcipomyiinae Up to 5 mm long. Body flattened, with long spine-like extensions (as in Fig. 8b) or rounded, with short lateral spines. Prolegs tipped with small dark spines. Marginally aquatic: damp soil at the water’s edge.

5. (3) Ventral prolegs present (at the front and/or rear of the body or at the front of the abdomen) 6

₋₋ Prolegs absent 10

6. Distinct swelling of the rear half of the abdomen; a single fused proleg at the front only

a) b)

Fig. 8. (a) Bibionidae; (b) Ceratopogonidae: subfamily Forcipomyiinae.

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Fig. 9. Simuliidae. Fig. 11. Ceratopogonidae: subfamily Dasyheleinae.

Simuliidae (blackflies)( Fig. 9) Up to 10 mm long. Basal pad of abdomen with many small hooks in a circular formation. Flowing waters only, where it attaches to solid substrates and submerged vegetation and can be abundant.

₋₋ Rear of abdomen no wider than thorax; prolegs not as above 7

7. Prolegs on the front two abdominal segments; body often bent into a U-shape (note: prolegs may be collapsed, but are clearly identifiable by the presence of rows of dark hooks on the front pair of abdominal segments) Dixidae (meniscus midges) (Fig. 10) Up to 8 mm long. Surface film amongst emergent vegetation in stream pools, ponds and wetlands.

₋₋ Prolegs on thorax and/or rear of abdomen, but not at the front of the abdomen 8

8. Prolegs present only at the rear of the abdomen, retractable into soft sheaths Ceratopogonidae – part: Dasyheleinae (Fig. 11) Up to 10 mm long. Marginally aquatic in ponds and upland springs.

₋₋ Prolegs both on the first segment of the thorax and at the rear of the abdomen 9

a) b)

Fig. 10. Dixidae: (a) with body extended; (b) with body in typical U-shape, seen in ventral view.

a) b)

Fig 12. Thaumaleidae: (a) whole animal; (b) close-up of head and front of thorax, showing spiracles and distinctive shape of head 9. A pair of spiracles on first thoracic segment (as inFig. 12b) and on dorsal side of last abdominal segment; anterior prolegs fused Thaumaleidae (trickle midges) (Fig. 12) Up to 15 mm long. Head a distinctive shape, with small bumps present on front (Fig. 12b). Very shallow water, rarely deeper than 3 mm, running over rock surfaces.

₋₋ No spiracles on thorax; anterior prolegs separate, although they may appear fused towards the base Chironomidae (Fig. 13) Up to 20 mm long but most less than 15 mm long. Every type of freshwater and brackish habitat, plus enclosed

Fig. 13. Chironomidae.

marine habitats (lagoons and docks); includes species adapted to living in grossly polluted water and species which live on intertidal rocks. 10. (5) Thorax clearly swollen relative to abdomen (as in Figs 14a, 16a) 11

₋₋ Thorax not swollen relative to abdomen 12

11. Antennae large and ending in stout hairs at least as long as the final antennal segment (as in Fig. 14b); silvery oval structures visible within the body cavity (as in Fig. 15) Chaoboridae (phantom midges) (Figs 14, 15)

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a) b)

Fig. 14. Chaoboridae: (a) whole animal; (b) close-up of head, showing distinct jointed antenna (arrowed).

Up to 12 mm long. Very pale or transparent (Fig. 15, although preserved specimens become opaque). Swimming larvae, in ponds, lakes and marshes.

₋₋ Antennae small and with hairs considerably shorter than final antennal segment (as in Fig. 16b) Culicidae (mosquitoes) (Fig. 16) Up to 12 mm long. Many have a hardened posterior siphon (breathing tube), as illustrated in Fig. 16a. Swimming larvae, in small still water bodies of all types, including temporary pools, tree holes and livestock drinking troughs.

Fig. 15. Chaoboridae: live animal in dorsal view. Fig. 17. Ptychopteridae.

a) b)

Fig 16. Culicidae: (a) whole animal, showing type with long posterior siphon; (b), close-up of head from the front, showing small unjointed antenna (arrowed).

12. (10) Posterior end with a long tapering siphon, often with two small oval structures (papillae) visible at its base; abdomen normally having the appearance of distinct circular rings, marking the raised edges of each segment Ptychopteridae (phantom craneflies) (Fig. 17) Up to 35 mm long. Shallow, muddy-bottomed or detritus-filled water; typically in saturated detritus at the edge of ponds and wetlands.

₋₋ No long siphon; no distinct appearance of rings around the abdomen 13

13. Body flattened in cross section, roughened, patterned with distinct lateral hairs and/or darkened plates 14

₋₋ Body slender and cylindrical in cross section, with little or no pigmentation or patterning 15

14. Dorsal surface with numerous transverse hardened plates and/or fringes of hairs along the sides; normally dark grey/ black in colour Psychodidae (moth flies or owl midges)( Fig. 18) Up to 30 mm long, but most less than half this length. Most very dark in appearance; generally elongated but a few more oval in shape. Marginally aquatic, in vegetation and detritus at the edge of ponds and streams.

₋₋ Dorsal surface roughened but without transverse plates; pale in colour, often with distinct patterning Stratiomyidae (soldier flies) (Fig. 19)

a) a)

Fig. 18. Psychodidae, dorsal view: (a) the typical form Fig. 19. Stratiomyidae, dorsal view: (a, b) examples of species (Psychodinae); (b) Sycoracinae, very small and rarely encountered, in which the circular tuft of hairs is present on the rear of the living in moss on the edge of small streams. abdomen; (c) example of a species in which the tuft of hairs is absent.

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Up to 55 mm long, although most considerably shorter. Most species have a distinctive ring of hairs at the posterior end, and many species have a pair of hooks on the ventral side towards the rear. Aquatic and marginally aquatic species, living in shallow water, normally in association with emergent vegetation.

15. (13)Abdominal segments divided so that there are apparently 21 body segments Ceratopogonidae: Leptoconopinae Up to 10 mm long. Southern Europe only. Head capsule not completely hardened.

Anisopodidae will key out here. The rear of its abdomen has a distinct ‘shield’ on the ventral side, and the head is hardened throughout. It is only recorded from tree holes. Up to 8 mm long.

₋₋ Body clearly comprising 12 segments 16

16. Each body segment considerably longer than wide; head long and slender; a tuft of hairs at the rear end of the abdomen Ceratopogonidae – part: Ceratopogoninae (Fig. 20a) Up to 15 mm long. No spiracles. Most are peripherally aquatic, in ditches and shallow marshes, but some occur in streams.

₋₋ Body segments less than 1.5 times as long as wide; head rounded; no tuft of hairs at the rear end of the abdomen. Scatopsidae (Fig. 20b) Up to 8 mm long. Rear end of abdomen with short extensions supporting spiracles, or with a semi-circular extension; spiracles visible along the abdomen. Tree holes.

Pachyneuridae will key out here. It has pairs of lateral spiracles on most of its body segments, and small swellings on the ventral sides of its thorax. Up to 10 mm long. Sweden and Finland only, in dead wood.

17. (1) Body flattened, with eight visible body segments, each with a distinct dorsal plate and with obvious long extensions at the anterior and posterior ends Lonchopteridae (Fig. 21) Up to 5 mm long. Peripherally aquatic: under stones at edge of rivers, particularly in gravel bars.

₋₋ Body not as above; more than eight visible segments, or segmentation unclear; no dorsal plates 18

18. Prominent soft extensions present, all along the body 19

₋₋ Extensions, if present confined to the rear end of the abdomen 20

a) a)

b) b)

Fig. 20. (a) Ceratopogonidae: subfamily Ceratopogoninae; (b) Scatopsidae. c)

Fig 22. (a) Cylindrotomidae: the very distinctive genus Phalacrocera, in dorsal view; (b) Cylindrotomidae: a terrestrial genus that occurs Fig. 21. Lonchopteridae, dorsal view in damp habitats; (c) Athericidae, in dorso-lateral view.

19. Extensions branched or toothed, arranged in longitudinal lines; prolegs absent Cylindrotomidae (Fig. 22a,b) Up to 30 mm long. Among vegetation in moss-filled pools.

₋₋ Extensions simple; distinct prolegs present; either two feather-like extensions to the rear of the abdomen (as in Fig. 22c) or five pairs of very long simple extensions from the rear segments (as inFig. 23) Athericidae (Figs 5a, 22c, 23) Up to 25 mm long. Rivers and streams.

20. (18) A single long extension, protruding from the rear end of the abdomen (including those in which the abdomen itself tapers into a long extension, as in Figs 24 and 25a); this extension may be simple (as in Figs 4a, 24) or may divide before its tip (as in Fig. 25) 21

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Fig 23. Athericidae: genus Atrichops, showing long extensions from the rear abdominal segments. Fig. 25. Ephydridae (a) type with prolegs; (b) example of type without prolegs. ₋₋ Not as above; extensions absent, or short and squat (as in Fig. 3a), or more than one 22

21. A single posterior extension, long (at least ¼ body length and often many times this) and flexible; prolegs may be present Syrphidae - part (Figs 4a, 24) Up to 20 mm long, not including the siphon, which can extend in some species to several times this length. Body with a distinctly wrinkled appearance; anterior (head end) does not narrow relative to the rest of the body. Standing waters with plenty of decaying vegetation, detritus-filled pools and tree holes.

₋₋ Rear extension divides into two before its tip (as in Fig. 25); prolegs may be present Ephydridae (part) (Fig. 25) Up to 18 mm long. Wetlands and shallow pools with vegetation, including salt marshes.

22. (20) Prolegs present (as in Figs 1a, 5a) 23

Fig. 24. Syrphidae: type in which the abdomen gradually tapers, shown in dorsal view.

a) b)

Fig. 26. (a) Pediciidae; (b) Empididae: rear of abdomen, dorsal view, of species with four short extensions; (c) Empididae: whole animal, showing a species without rear extensions.

₋₋ Prolegs absent 25

23. Four or five pairs of prolegs (if four, may be reduced to short protrusions); a single pair of narrow backwards-directed extensions at the rear end of the abdomen Pediciidae (Figs 1a, 26a) Up to 50 mm long although most are less than 20 mm long. Pools and shallow trickles, and commonly in streams and shallow rivers.

₋₋ Six to eight pairs of prolegs; normally either 2-4 short extensions at the rear end of the abdomen, or none; if two narrow dorsal extensions, these curve to face forwards (as in Fig. 3b) 24

24. Seven or eight pairs of prolegs; either 3-4 short backward-pointing extensions at the rear end of the abdomen (as in Fig. 26b), or none (as in Fig. 26c) Empididae (Fig. 26b, c) Up to 7 mm long. The rear prolegs are larger than the others and often project sideways (as in Fig. 26b). Rivers and streams.

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Fig. 27. Limoniidae: example of a genus with a flattened spiracular Fig. 28. Rhagionidae: ventral view of rear of abdomen, showing disc encircled by five short lobes. the V-shaped ridge around the anal area (vr), and the ridges encircling the abdominal segments (ar). ₋₋ Six pairs of prolegs plus a pair of long ventral extensions at the rear end of the abdomen (as in Fig. 3b); two dorsal extensions that curve to face forwards (as in Fig. 3b) Muscidae – part (Fig. 3b) This has been included here because one genus has extensions to its abdominal segments that can be interpreted as short prolegs. See couplet 40 for more details.

25. (22) Rear of abdomen with tufts of long golden- or copper-coloured hairs on four lobes (as in Fig. 6b); lobes may be closed into a conical shape (as in Fig. 34d) Limoniidae – part Up to 22 mm. Often covered in fine hairs, giving a downy appearance. The general body form of Limoniidae is illustrated in Fig. 34c. Shallow vegetated water bodies, wetlands and stream edges.

₋₋ Rear of abdomen lacks tufts of very long hairs, although shorter hairs and/or prominent lobes may be present 26

26. Abdomen has dorsal and ventral welts (as in Figs 5b, 6c) or ventral welts only (as in Fig. 6d), or distinct hardened protuberances (as in Fig. 3a) or ridges (as in Figs 3a, 28) encircling the body 27

₋₋ Welts or encircling protuberances absent 29

27. Abdominal segments with dorsal and ventral welts (distinct if dark, as in Fig. 5b, but may be pale and difficult to see, as in Fig. 6c), or with ventral welts only (as in Fig. 6d); either two long extensions at the rear of the abdomen (as in Fig. 5b) or a flattened end with two prominent spiracles (as in Figs 6c, 27) Limoniidae – part

Up to 22 mm long. Includes a wide variety of different forms: the distinctive genusAntocha (Fig. 5b), which lacks spiracles; plus others with five conical lobes; five very short lobes (as inFig. 27) or completely lacking lobes (as in Fig. 6c). Antocha lives in tubes under stones in streams; the others are mainly found in shallow vegetated ditches, wetlands, tree holes and peripheral habitats, including some in saturated rotting wood.

₋₋ Abdominal segments encircled by rings of hardened protuberances; rear of the abdomen either with a single upward-angled squat appendage (as in Fig. 3a) or four lobes of equal length around a spiracular disc; an oval or V shaped ridge around the anal area on its ventral side (as in Fig. 28) 28

28. A single squat appendage on the dorsal side of the last abdominal segment Tabanidae (horseflies) (Figs 3a, 29a) Up to 40 mm long, although most smaller than 25 mm. Peripherally aquatic, in small trickles and the edges of streams.

₋₋ Last abdominal segment with four short lobes of equal length around a spiracular disc Rhagionidae (Figs 28, 29b) Up to 12 mm long. Peripherally aquatic in damp vegetation, although occasionally collected in stony streams.

29. (26) Abdomen ends in one or two short piercing spines 30

Fig. 29. (a) Tabanidae; (b) Rhagionidae.

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b) c)

Fig. 30. (a,b) Ephydridae, showing a species with respiratory lobes modified into piercing spines: (a) whole animal, ventral view; (b) close up of rear of abdomen; (c) Limoniidae, detail of the rear of the abdomen of a type with two small diverging hooks.

₋₋ Rear of abdomen without spines 32

30. Abdomen ends in a single spine, on the end of a short appendage. Syrphidae – part (Fig. 4b) Up to 10 mm long. Body wrinkled in appearance. The distinctive genus Melanogaster, which uses its spine to pierce aquatic plants in order to obtain oxygen. Well vegetated shallow water.

₋₋ Abdomen ends in a pair of spines, flush with the end of the segment 31

31. Body short and flattened. Spines situated on a truncate rear abdominal segment (as inFig. 30a, b) Ephydridae – part (Fig. 30a,b) Up to 6 mm long. Aquatic plants in wetlands and shallow pools, often living within the leaves.

₋₋ Body elongated and cylindrical. Spines situated on a narrowing rear abdominal segment (as in Fig. 30c) Limoniidae – part

a) b)

Fig. 31. Sciomyzidae: (a) whole animal, dorsal view; (b) posterior of abdomen, showing paired structures with branched filaments covering the spiracles.

Up to 20mm long. At least one genus has two rear hooks that may be interpreted as spines. The general body form of Limoniidae is illustrated in Fig. 34c. Vegetated wetlands.

32. (29) Rear end of abdomen with an obvious disc containing a pair of spiracles (visible as darkened circles or ovals, as in Fig. 33b, although they may be covered, as in Fig. 31b) and normally (but not always!) surrounded by lobes. Note: if spiracles are not clearly visible but lobes are present, as in Figs 6a, 34b, then choose this option 33

₋₋ No spiracular disc; spiracles on the end of extensions or not clearly apparent 40

33. Spiracles covered by a pair of circular features with branched filaments (as inFig. 31b) Sciomyzidae (snail-killing flies) (Fig. 31) Up to 20 mm long. Body heavily wrinkled; anterior (head) end narrows relative to the rest of the body. Standing waters in vegetation; associated with aquatic snails, upon which they feed.

₋₋ Spiracles not as above, consisting of simple circular structures 34

Fig. 32. Scathophagidae.

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34. Posterior of abdomen with a large number of very short lobes around a flat posterior end that is orientated at a slight angle relative to the plane of the body Scathophagidae (Fig. 32) Body generally covered with small spines. Up to 10 mm long. Peripherally aquatic, in detritus at the edge of water bodies.

₋₋ Posterior of abdomen not as above; flat posterior end surrounded by no more than six lobes (do not confuse lobes around the spiracles with anal papillae, which extend from underneath the spiracular disc – see Figs 6b, 33b) 35

35. Rear end of abdomen with six lobes around the spiracular disc Tipulidae (craneflies)( Fig. 33) Up to 60 mm long. Decaying vegetation in various freshwater habitats, including streams, wetlands, lake edges and damp peripheral habitats; sometimes in saturated rotting wood.

₋₋ Rear end of abdomen with five or fewer lobes around the spiracular disc 36

36. Spiracular disc lacking lobes (Fig. 6c) Limoniidae – part (Fig. 6c) This has been included here because its welts may be overlooked. See couplet 27 for more details.

₋₋ Four or five lobes present around the spiracular disc (as inFigs 27, 34a) 37

37. Five spiracular lobes present, often with areas of dark patterning (as inFig. 34a) Limoniidae – part Up to 20 mm long. May be covered in fine hairs, giving a downy appearance. The general body form of Limoniidae is illustrated in Fig. 34c. Mostly in small trickles and in peripheral habitats; sometimes in saturated rotting wood.

a) b) s

Fig. 33. Tipulidae: (a) whole animal; (b) posterior end with spiracles, s, lobes, l, and anal papillae, ap, arrowed.

a) b)

Fig. 34. Limoniidae (a) posterior end, dorsal view, showing a species with five lobes; (b) posterior end, ventral view, showing a species with four lobes; (c,d) whole animal (c) and posterior end (d) showing a species lacking clear lobes but with a distinct tuft of long curved hairs.

₋₋ Four spiracular lobes present 38

38. Rear end of abdomen with four long cylindrical lobes around the spiracular disc (as in Fig. 34b), often with distinct tufts of hairs growing on them (as in Fig. 6b) Limoniidae – part

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Fig. 35. Dolichopodidae.

Fig. 36. Cecidomyiidae, ventral view.

Up to 20 mm long. May be covered in fine hairs, giving a downy appearance. The general body form of Limoniidae is illustrated in Fig. 34c. Small streams, stream edges and vegetated shallow water.

₋₋ Rear end of abdomen with four short lobes, approximately triangular in shape and lacking distinct hairs, around the spiracular plate 39

39. Lobes at end of abdomen all similar in length; an oval or V shaped ridge around the anal area on its ventral side (as in Fig. 28) Rhagionidae (Fig. 28, 29b) This has been included here because its encircling protuberances may be overlooked. See couplet 28 for more details.

₋₋ Ventral lobes at end of abdomen longer than dorsal lobes; no obvious structure around the anal area Dolichopodidae (Fig. 35) Up to 10 mm long. Wet soil, mud and damp moss, including some in salt marshes and sea shore habitats.

40. (32) Rear end of abdomen with a pair of long dorsal extensions that curve forwards, plus a similar pair of ventral extensions (as in Fig. 3b) Muscidae – part (Fig. 3b) Up to 16 mm long. The spiracles are situated on the ends of the dorsal extensions. Commonly encountered in stony streams.

₋₋ Rear end of abdomen lacking extensions of this type, although short lobes and/or tufts of hairs may be present 41

41. Rear end of abdomen with distinct tufts of hairs (as in Fig. 34d) Limoniidae – part (Fig. 34 c,d) Up to 20 mm long. May be covered in fine hairs, giving a downy appearance. Mostly in peripheral habitats, occasionally straying into open water.

₋₋ Rear end of abdomen without distinct tufts of hairs 42

42. Body slightly flattened; a distinct pigmented mark on the underside of the thorax (as in Fig. 36) Cecidomyiidae (Fig. 36) Up to 6 mm long. Aquatic habitat poorly known, but likely to be peripheral; mainly recorded from stream edges.

₋₋ Body cylindrical, and lacking the distinct pigmented mark 43

43. Rear end of abdomen with a pair of short rounded extensions that are orientated slightly dorsally (as in Fig. 37a) Muscidae - part (Fig. 37) Up to 12 mm long. Mud in shallow ponds and lakes, and in tree holes.

₋₋ Rear end of abdomen with a pair of small hooks (as in Fig. 30c), or apparently lacking any features Limoniidae – part Up to 22 mm long. The general body form of Limoniidae is illustrated in Fig. 34c. Mostly in peripheral habitats and shallow vegetated wetlands.

a) b)

Fig. 37. Muscidae: (a) whole animal; (b) posterior end in dorsal view, with short spiracular extensions.

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Acknowledgments Dahlem, G.A. & Naczi, R.F.C. (2006). Flesh flies (Diptera: Sarcophagidae) associated with North American pitcher plants I thank Rachael Carrie (Lancaster University) for supply (Sarraceniaceae), with descriptions of three new species. Annals of Cecidomyiidae, James Pretty (Queen Mary University of the Entomological Society of America 99, 218-240. of London) for supply of Bibionidae, and Dmitri Logunov Derraik, J.G.B. & Heath, A.C.G. (2005). Immature Diptera (Manchester Museum) for access to Allan Brindle’s (excluding Culicidae) inhabiting phytotelmata in the Auckland collection of Diptera larvae. I am also grateful to Malcolm and Wellington regions. New Zealand Journal of Marine and Elliot and to an anonymous reviewer for constructive Freshwater Research 39, 981–987. comments that improved this key immensely. Disney, R.H.L. (1991). The Aquatic Phoridae (Diptera). All line drawings are taken from Dobson et al. (2012), Entomologica Scandinavica 22, 171-191. other than Fig. 20b (from Laurence, 1953), Fig. 21 (from Disney, R.H.L. (1995). Further new species of aquatic Phoridae Drake, 1996) and Figs 7, 8a, 26b, 30c and 36 (originals (Diptera) from Malaysia and Brunei. Aquatic Insects 17, 205-213. by M. Dobson). All photographs are by M. Dobson. Disney, R.H.L (1999). British Dixidae (Meniscus Midges) and Thaumaleidae (Trickle Midges): Keys with Ecological Notes. References Scientific Publication No. 56. Freshwater Biological Association, Ambleside. 129 pp. Bass, J. (1998). Last-instar Larvae and Pupae of the Simuliidae of Britain Disney, R.H.L., Copeland, R.S. & Murrell, E. (2009). The true and Ireland. A Key with Brief Ecological Notes. Scientific Publication identity of Copeland’s aquatic scuttle fly (Diptera: Phoridae) No. 55. Freshwater Biological Association, Ambleside. 102 pp. from Indiana and recognition of a sibling species from Texas. Bertrand, H. (1954). Les Insectes Aquatiques d’Europe, Vol. Proceedings of the Entomological Society of Washington 111, II. – Trichoptères, Lépidoptères, Diptères, Hyménoptères. Paul 564-4574. Lechevalier, Paris. 547 pp. Dobson, M., Pawley, S., Fletcher, M. & Powell, A. (2012). Guide Brauer, F. (1883). Die Zweiflüger des Kaiserlichens Museums to Freshwater Invertebrates. Scientific Publication No. 68. zu Wien. III Systematische Studien auf Grundlage der Freshwater Biological Association, Ambleside. 216 pp. Dipteren-Larven nebst einer Zusammenstellung von Drake, C.M (1996). The larva and habitat of Lonchoptera nigrociliata Biespielen aus der Literatur über dieselben und Beschreibung (Diptera: Lonchopteridae). Dipterists Digest 3, 28-31. neuer Formen. Denkschriften der Kaiserlichen Akademie der Dudley, T. & Anderson, N.H. (1982). A survey of invertebrates Wissenschaften, Mathematisch-Naturwissenschaftliche Klasse 47, associated with wood debris in aquatic habitats. Melanderia 39, 1-100. [NB. Date cited in older literature as 1883, but appears in 1-21. Zoological Record for 1884.] Fauna Europaea (2013). Fauna Europaea. http://www.faunaeur. Borkent, A. & Rotheray, G. (2009). Key to Diptera families – org. Accessed March 2013. larvae. In: Manual of Central American Diptera, Volume 1 (eds B.V. Fish, D. & Hall, D.W. (1978). Succession and stratification of Brown, A. Borkent, J.M. Cumming, D.M. Wood, N.E. Woodley aquatic insects inhabiting the leaves of the insectivorous pitcher & M.A. Zumbado), pp. 157-191. NRC Research Press, National plant, Sarracenia purpurea. American Midland Naturalist 99, Research Council of Canada, Ottawa. 172-183. Brindle, A. & Smith, K.G.V. (1978). The Immature Stages of Flies. Fitter, R. & Manuel, R. (1986). Collins Field Guide to Freshwater Life. In: A Dipterist’s Handbook (eds A. Stubbs & P. Chandler), pp. Collins, London. 382 pp. 38-64. The Amateur Entomologists’ Society, Hanworth. Fitzgerald, S.J. (2005). Evolution and Classification of Bibionidae Churchel, M.A. & Batzer, D.P. (2006). Recovery of (Diptera: Bibionomorpha). PhD thesis, Oregon State University, macroinvertebrate communities from drought in Georgia USA (unpublished). Piedmont headwater streams. American Midland Naturalist 156, Godfrey, A. (1999). A review of Diptera from exposed riverine 259-272. sediments based on literature records. Dipterists Digest 6, 63-82.

Gooderham,J. & Tsyrlin E. (2002). The Waterbug Book. A Guide to organisation. Oecologia 90, 172-184. the Freshwater Macroinvertebrates of Temperate Australia. CSIRO Mogi, M. & Chan, K.L. (1996). Predatory habits of dipteran larvae Publishing, Collingwood, Vic. 232 pp. inhabiting Nepenthes pitchers. Raffles Bulletin of Zoology 44, Haenni, J-P. & Vaillant, F. (1994). Description of dendrolimnobiotic 233-245. larvae of Scatopsidae (Diptera, Nematocera) with a review of Oscoz, J., Galicia, D. & Miranda, R. (Eds.) (2011). Identification our knowledge of preimaginal stages of the family. Mitteilungen Guides of Freshwater Macroinvertebrates of Spain, Springer, der Schweizerischen Entomologischen Gesellschaft 67, 43-59. Dordrecht. 153 pp. Meillon, B. de & Werth, W.W. (2003). Ceratopogonidae. In: Guides Salmela, J. Autio, O. & Ilmonen, J. (2007). A survey on the to the Freshwater Invertebrates of Southern Africa. Volume 9: Diptera nematoceran (Diptera) communities of southern Finnish (eds J.A. Day, A.D. Harrison & I.J. de Moor), pp. 50-56. Water wetlands. Memoranda Societatis pro Fauna et Flora Fennica 83, Research Commission, Gezina (South Africa). 33–47. Hennig, W. (1948). Die Larvenformen der Dipteren. Vol. 1. Skartveit, J. (2002). The larvae of the European Bibioninae (Diptera, Akademie Verlag, Berlin. 185 pp. Bibionidae). Journal of Natural History 36, 449-485. Hennig, W. (1950). Die Larvenformen der Dipteren. Vol. 2. Smith, K.V. (1989). An Introduction to the Immature Stages of British Akademie Verlag, Berlin. VII + 458 pp. Flies. Royal Entomological Society Handbooks for the Identification Hennig, W. (1952). Die Larvenformen der Dipteren. Vol. 3. Akademie of British Insects, Vol. 10, Part 14. British Museum (Natural Verlag, Berlin. VII + 628 pp. History), London. 280 pp. Johannsen, O.A. (1934). Aquatic Diptera. Part I. Nemacera [sic], Smith, K.V. (1997). Diptera, Introduction to immature stages. In: exclusive of Chironomidae and Ceratopogonidae. Memoir 164. The Aquatic Insects of North Europe Volume 2 (ed. A. Nilsson A), Cornell University Agricultural Experiment Station, Ithaca. 95 pp.79-92. Apollo Books Stenstrup. pp. Sota, T. & Mogi, M. (1996). Species richness and altitudinal Johannsen, O.A. (1935). Aquatic Diptera. Part II. Orthorrhapha- variation in the aquatic metazoan community in bamboo Brachycera and Cyclorrhapha. Memoir 177. Cornell University phytotelmata from North Sulawesi. Researches on Population Agricultural Experiment Station, Ithaca. 74 pp. Ecology 38, 275-281. Kitching, R.L. (1969). A preliminary note on the fauna of Sundermann, A., Lohse, S., Beck, L.A. & Haase, P. (2007). Key water-filled tree holes. The Entomologist 102, 7-9. to the larval stages of aquatic true flies (Diptera), based on the Laurence, B.R. (1953). The larva of Ectaetia (Diptera: Scatopsidae). operational taxa list for running waters in Germany. Annales de Entomologists’ Monthly Magazine 89, 204-205. Limnologie 43, 61- 74. Louton, J., Gelhaus, J. & Bouchard, R. (1996). The Tachet, H., Bournaud, M. & Richoux, Ph. (1980). Introduction aquatic macrofauna of water-filled bamboo (Poaceae: à l’Etude des Macroinvertébrés des Eaux Douces (Systématique Bambusoidaceaea: Guadua) internodes in a Peruvian lowland élémentaire et aperçu écologique). Université Lyon 1, Villeurbanne. tropical forest. Biotropica 28, 228-242. 155 pp. Macan, T.T. (1959). A Guide to Freshwater Invertebrate Animals. Tachet, H., Richoux, Ph., Bournaud, M. & Usseglio-Polatera, Ph. Longmans, London. 118 pp. (2010). Invertébrés d’Eau Douce. Systématique, biologie, écologie. Malloch, J.R. (1917). A preliminary classification of Diptera, CNRS Editions, Paris. 587 pp. exclusive of pupiparia, based on larval and pupal characters, Thomas, A.G.B. (1980). Diptères torrenticoles peu connus: VII. with keys to imagines in certain families. Part 1. Bulletin of the Les Cecidomyiidae Porricondylinae du sud-ouest de la France Illinois State Laboratory of Natural History 12, i-v, 161-409, plates (Nematocera). Annales de Limnologie 16, 225-231. 28-62. Vaillant, F. (2002). Insecta: Diptera: Lonchopteridae. In: Mogi, M. & Yong, H.S. (1992). Aquatic arthropod communities Süsswasserfauna von Mitteleuropa, Vol. 21, Insecta, Diptera, 22, 23, in Nepenthes pitchers: the role of niche differentiation, Lonchopteridae, Sciomyzidae (eds J. Schwoerbel & P. Zwick ), pp. aggregation, predation and competition in community 1-14. Spektrum Akademischer Verlag, Heidelberg.

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Author Profile Michael Dobson has a keen interest in enhancing skills in identifying freshwater invertebrates, and has recently written or co-authored several identification guides, on invertebrates in general, freshwater shrimps (Amphipoda) and freshwater Diptera. In addition to researching the ecology of streams and wetlands of Europe and Africa, he has taught identification skills for around 20 years, most recently on courses run by the Freshwater Biological Association (FBA). After six years as Director of the FBA, he moved in May 2013 to APEM Ltd, where he is now Principal Freshwater Consultant.