NEW RECORDS OF TRICHOPTERA IN REFERENCE MEDITERRANEAN-CLIMATE RIVERS OF THE IBERIAN PENINSULA AND NORTH OF AFRICA: TAXONOMICAL, FAUNISTICAL AND ECOLOGICAL ASPECTS

Trichoptera is a very rich order in the Western Mediterranean, but knowledge of caddisflies in the Iberian Peninsula and northern Africa is still not complete. We present records of caddisflies collected in 114 sites of the Mediterranean climate region of the Iberian Peninsula and the western Rif. We also provide notes on ecological aspects and taxonomical remarks on some species. A total of 86 species were identified and 8 species extended their distribution range. Considering the four differentiated geological regions in the western Mediterranean Basin during the Tertiary, 60 species were collected in the Iberian plate region, 29 in the Transition, 30 in the Betic and 18 in the Rif. Local richness was not significantly different between the four regions but significant differences were found among several river ecotypes within regions. Temporary sites had lower local richness than other ecotypes in all regions except in the Rif, whereas headwaters had similar richness in any region regardless of their geology. The Rif region had the lowest Trichoptera richness, which is not only the result of the scarcity of faunistic studies in the area but also of the high frequency of temporary rivers and the isolation of the area. Our results suggest that conservation measures addressed to preserve the biodiversity of the Western Mediterranean should be enforced, especially in the Rif region.


Introduction
The Mediterranean Basin has been considered a hotspot of biodiversity, at least when looking at plants and vertebrates (Myers et al., 2000).Insects are also diverse in the area especially when considering the reduced dimensions of the emerged land (Balleto & Casale, 1989).In particular, the western Mediterranean, and specially the south of the Iberian Peninsula and the north of Morocco (i.e.Betic-Rif ranges), is one of the two main centres of biodiversity within the Mediterranean Basin (Médail & Quézel, 1997).Likewise, Trichoptera is a very rich order in the Western Mediterranean, with about 390 species in the Iberian Peninsula (González, 2007) and 72 in Morocco (Dakki, 1980).In spite of having a high caddisfly richness, the knowledge of caddisflies in the Iberian Peninsula and north of Africa is still incomplete, new species are still recorded and many larval stages are not yet described (e.g.González & Ruiz, 2001;Zamora-Muñoz et al., 2002, 2006).Consequently, general studies providing information about caddisflies are required in both areas to have a consistent taxonomy of the group which will help to carry out proper ecological studies or to promote specific conservation measures.
Thus, our main aim was to complement the existing information (e.g.Dakki, 1980;González et al., 1992;Vieira-Lanero, 2000;Ruiz et al., 2001;Bonada et al., 2004b) with new records.The study area broadly corresponds to that studied in Bonada et al. (2004b) but with new sites and basins, including those found in the western Rif.The caddisfly records presented follow the taxonomical classification described in Wiggins (1996) and are updated using Fauna Iberica (www.fauna-iberica.mncn.csic.es)and Fauna Europaea (www.faunaeur.org)web services.In addition, we follow the traditional species terminology and escape from recent synonyms without a consistent study of the species implied (Botosaneanu, in letter to C. Zamora-Muñoz, 2005).In some cases, we also provide taxonomical notes.Notes on ecological aspects of the species not already included in Bonada et al. (2004b) are given by using information compiled by the Guadalmed project (see www.ecostrimed.net)or by using references provided in Table 1.
Several authors have suggested that a mixture of complex past historical processes occurring during the Tertiary and Quaternary with current heterogeneous environmental conditions are responsible for the high biodiversity found in the Mediterranean Basin (Balleto & Casale, 1989;Hewitt, 2004;Bonada et al., 2005).Among historical factors, those that occurred during the Tertiary in the western Mediterranean Basin resulted in four differentiated geological regions: Iberian Plate, Transition, Betic and Rif.Among ecological factors, basin geology, river zonation and seasonal variability are the most relevant to understand caddisfly distribution (Bonada et al., 2005).Both groups of factors have implications on regional richness which in turn influences local richness (Vinson & Hawkins, 2003).We will analyze Trichoptera from these geological regions in terms of regional (i.e.richness in each geological region) and local richness (i.e.richness in each site).Given that basin geology and river zonation are the main environmental factors constraining caddisflies Sesenta especies se recolectaron en la región de la placa Ibérica, 29 en la de Transición, 30 en la Bética y 18 en el Rif, las cuatro regiones geológicas diferenciadas durante el Terciario en el Mediterráneo Occidental.La riqueza local no fue significativamente diferente entre regiones geológicas, pero sí entre varios ecotipos fluviales.Los tramos temporales presentaron una riqueza local menor que los demás ecotipos, excepto en el Rif, mientras que las cabeceras presentaban una riqueza similar en cada región independientemente de su geología.Globalmente el Rif presentó una menor riqueza de tricópteros, lo que se explica no sólo por la escasez de estudios faunísticos en la zona sino también por la elevada frecuencia de ríos temporales y su aislamiento geográfico.Nuestros resultados sugieren que en la zona del Mediterráneo Occidental se deben de llevar a cabo medidas de conservación urgentes para preservar su biodiversidad, especialmente en la región del Rif.

Material and methods
We collected Trichoptera specimens from 114 sites belonging to 28 basins.All sites were considered as reference regarding their ecological quality (Bonada et al., 2004a) and located in different river sections (i.e.headwaters, midstreams and lowland reaches) with different basin geology (i.e.calcareous, siliceous or sedimentary) and at different altitudes (from 20 to 1940 m.a.s.l., Appendix).Our study was focused within the limits of the Mediterranean climate established by Köppen (1931) and covered a sampled area of 70854.12km 2 , from the northeast of the Iberian Peninsula to the western Rif zone in Morocco (Fig. 1).The sampled area was divided into 4 different geological regions: the Iberian Plate (42 sites), the Transition zone (9 sites), the Betic (43 sites) and the Rif zones (20 sites).The Iberian Plate comprises the area of the Iberian Peninsula which includes the Hesperic Massif (west of the Iberian Peninsula which originated in the hercinic orogeny during the Carboniferous), the Iberian Ranges (east of the Hesperic Massif with a hercinic base and a sedimentary cover) and the Catalan Ranges (northeast of the Hesperic Massif with a hercinic and alpine orogeny origin and a sedimentary cover).The Transition zone is equivalent to the Prebetic area, located in the external zone of the Betic Ranges and originated, before the collision of the Betic-Rif microplate, by marine deposits or terrestrial sediments from the Iberian Plate.The Betic zone encloses the Internal Zone of the Betic Ranges (also called Betic s.s.), which was part of the Betic-Rif microplate, and the flychs deposits, coming from eastern areas and reached the Strait of Gibraltar with the migration of the Betic-Rif microplate (Sanz de Galdeano & Vera, 1991).Likewise, the Rif zone comprises the Internal zone and the flychs deposits of the Rif Ranges (Fig. 1).
In each site, we sampled all available habitats with a kick net of 250-300 µm mesh size depending on the survey, until no new caddisfly families were observed in the field.Samples were preserved in formalin (4%) or alcohol (96%) and identified to the species level in the laboratory.In addition, lastinstar larvae and pupa were collected in the field and reared in the laboratory to obtain adults for ensuring larval identifications (for the method used see Bonada et al., 2004b).When possible, adults were also obtained in the field by sweeping riparian vegetation with an entomological net or by using a UV-light trap.
Local richness referred to the number of species collected at each site.In order to check local richness of caddisflies between ecotypes within geological regions we performed a nested ANOVA.Residuals were checked for normality and homogeneity of variances using Shapiro-Wilk and Bartlett tests, respectively.The nested design included 2 fixed factors nested as follows: ecotype nested to geological region.Although nested ANOVA designs usually use random nested factors, fixed factors can also be used (Quinn & Keough, 2002).As mentioned, the geological region factor includes: Iberian Plate, Transition, Betic and Rif.Regarding ecotypes, we used those developed for Mediterranean Basin rivers in Sánchez-Montoya et al. (2007): (1) temporary streams, (2) evaporite calcareous streams at medium altitude, (3) siliceous headwaters at high altitude, (4) calcareous headwaters at medium and high altitude and (5) large watercourses (Appendix).These statistical analyses were performed using the R freeware (http://www.r-project.org/).

Results
A total of 4041 larvae, 25 pupae and 131 adults were collected in the sampled area.Most of them were identified at species level, resulting in 86 different species.For each species, information of number of larva (L), pupae (P) and adults (m and f) collected are provided.For mature pupae and adults, the months of capture are presented in brackets after the locality.When the identity of the identification was not clear, a question mark (?) is added before some sampling sites or number of specimens.Sites are arranged by latitude of the whole basin (Fig. 1) and information about geographical position and general environmental characteristics of each locality is found in the Appendix.Larvae found corresponded to this species but there is controversy about the presence of this species in the Iberian Peninsula (see Bonada et al., 2004b).Rhyacophila fonticola Giudicelli & Dakki, 1984 MATERIAL STUDIED: 10L.Martil: R14; Laou: R3, R4, R8 See comments for Rhyacophila munda.

Rhyacophila rupta
Family GLOSSOSOMATIDAE Wallengren, 1891Subfamily Agapetinae Martynov, 1913Agapetus Curtis, 1834 As reported before (Bonada et al. 2004b) this genus contains one species with undescribed larvae present in our sampled area (Agapetus theischingeri Malicky, 1980).In addition, most of the morphological characters used to distinguish species use lateral and ventral abdominal setae patterns (e.g.see Pitsch, 1993).This may yield misidentifications because these setae may be broken or not clearly visible.For example, two specimens found in Tajo Basin (H5) had only one lateral seta in the first abdominal segment and very few dorsal setae in the ninth abdominal sclerite.Given this difficulty, here we only present specimens with larvae that fit in the known species and from sites where pupae or adults have been collected previously (Bonada et al., 2004b).McLachlan, 1884 MATERIAL STUDIED: 33L, 1P.Laou: R13 (1Pm: V-2005).Genil: B10, B12, B13, B15, B18, B19; Verde: B35; Martil: R14; Adelmane: R15, R16 Ruiz et al. (2004) reported that larva of A. incertulus does not have ventral setae in the sixth and seventh segments.Although most of our specimens followed this character (as well as the others characteristics of this species), some specimens in B13 and B15 had ventral setae in at least one of these segments.

Hydroptila Dalman, 1819
We collected 178 larva specimens belonging to this genus but because many immature forms of Iberian species remain undescribed, we only present here results from sites where pupa or adults of the species were found.Oxyethira Eaton, 1876 Three specimens from this genus have been found in Francolí (H35), Júcar (T3) and Guadalfeo (B25) basins.Given the difficulties of identifying larvae, we did not reach species level.

Tribe Orthotrichiini Nielsen, 1948 Ithytrichia Eaton, 1873
Three specimens of this genus (not identifiable at species level because of the scarcity of published information on larval morphology, Vieira-Lanero, 2000) were found in the Guadiana Basin (H11).

Tinodes Curtis, 1834
As pointed out in Bonada et al. (2004b) several species of this genus present in the area of study are not described and records presented here should be confirmed, except in cases where adults are found.

Polycentropus kingi
The presence of this species in T8 is confirmed by adult collection in previous studies (Zamora-Muñoz et al., 2002).

Brachycentrus (B.) subnubilus
The presence of this species in T8 has been confirmed previously by adult collection (Zamora-Muñoz et al., 2002).

Anomalopterygella Fischer, 1966
Anomalopterygella chauviniana (Stein, 1874) MATERIAL STUDIED: 16L.Guadiana Menor: B27; Genil: B9; Adra: B2, B3; Guadalfeo: B20, B26 Until now, A. esparraguera, one of the eight species of this genus present in the Iberian Peninsula, had been recorded only in Sierra Nevada (Schmid, 1952a;b) and Sierra de Cazorla (Sipahiler, 1998).With this record of Sierra de Baza, we extend its distribution to other areas of the Betic Ranges.All Annitella species are rare and only the larva of A. obscurata (McLachlan, 1876) has been described (e.g.Vieira-Lanero, 2000), thus the genus is seldom included in larval keys.The larvae collected in this site were small (III instar) and fitted with Halesus or Chaetopteryx following the keys of Vieira-Lanero (2000) and Camargo & García de Jalón (1988).

Local richness
From the 86 species identified with certainty in this study, 60 species were present in the Iberian plate region, 29 in the Transition, 30 in the Betic and 18 in the Rif.Although Rif showed the lowest regional species richness, local richness was not significantly different between geological regions (F-value = 2.457, p = 0.068).Significant differences were however found between ecotypes within regions (F-value = 4.097, p = 0.004).Residuals did not significantly differ from normality (p = 0.70) and from homogeneity of variances (p > 0.160).Box-plots indicated that temporary sites (Fig. 2) had lower local richness than other ecotypes in all regions except in the Rif.Headwaters, regardless of their geology, had similar richness and, when present, richness in lowland sites was also similar to that present in headwaters.

Discussion
Our work complements records reported in previous studies in the Mediterranean climate region of the Iberian Peninsula and north Africa (e.g.Dakki, 1980;Ruiz et al., 2001;Bonada et al., 2004b) with information from several not previously studied sites.We have found 22 species not recorded in Bonada et al. (2004b), 4 of them only found in the Rif.Information about the distribution of these species and their ecological requirements is provided in Table 1.In addition, comparing with González et al. (1992) and Bonada et al. (2004b) we provide records that extend the distribution of several species in the Mediterranean area of the Iberian Peninsula.Glossosoma boltoni, Allogamus ligonifer, Lepidostoma hirtum and Lacarsia partita were recorded in the southern basins.Brachycen-trus (B.) montanus, Rhyacophila meridionalis and Limnephilus lunatus were also present in central basins.Calamoceras marsupus was also collected in northern basins.
Graellsia, 64(2), Diciembre 2008, pp.189-208 -ISSN: 0367-5041 Coleoptera, Bennás et al., 1992;Ribera, 2000).However, the Rif has been considered an isolated area (Jolly et al., 1998;Cosson et al., 2005), which makes the maintenance of a diverse freshwater fauna more difficult.This is even more problematic for caddisflies, which are not equipped with biological strategies to cope with the frequent summer droughts of the region (Littmann, 2000;Williams, 2006).This observation is in accordance with the lowest local caddisfly richness recorded in the ecotype 1 that we found in all geological regions except in the Rif.All this suggestd that conservation measures have to be enforced in this area to preserve its biodiversity.
Several authors have pointed out the importance of large-scale characteristics on macroinvertebrate distributions (e.g.Sandin & Johnson, 2004).In particular, basin geology and river zonation were considered, among several environmental variables, the most important to explain caddisfly distribution in the Mediterranean climate rivers of the Iberian Peninsula (Bonada et al., 2005).Basin geology determines mineralization of water and river zonation results in changes in the hydraulic forces, the terrestrial influence and the resources available among others (Hawkins & Sedell, 1981;Statzner et al., 1988;Leland & Porter, 2000).However, although these parameters constrain caddisfly distribution, our results show that taxa richness is maintained between ecotypes with permanent flow conditions.This observation contrasts with other studies in temperate Europe using caddisflies that recorded an increase of species with surrogates of river zonation, such as stream width and slope (Wiberg-Larsen et al., 2000).The higher biodiversity of caddisflies in the Western Mediterranean compared to temperate Europe (e.g.around 200 species in Denmark and England, but almost double in the Iberian Peninsula, Wallace et al., 1990;González et al., 1992;Edington & Hildrew, 1995;Wiberg-Larsen et al., 2000) is probably accountable to this observation.
Graellsia, 64(2), Diciembre 2008, pp.189-208 -ISSN: 0367-5041 Appendix.-Location of the sampled sites in the Iberian Peninsula and the Rif.For each site the code used in the text, UTM coordinates, altitude, river name, geographical province and ecotype are shown.Ecotype refers to the categories provided by Sánchez-Montoya et al. (2007) and corresponds to: (1) temporary streams, (2) evaporite calcareous streams at medium altitude, (3) siliceous headwaters at high altitude, (4) calcareous headwaters at medium and high altitude and (5) large watercourses.Sites are arranged by alphabetical order of "Code".

Fig. 1 .
Fig. 1.-Site location and sampling area grouped by geological regions: Iberian Plate, Transitional, Betic and Rif zones.The boundary of the Mediterranean climate according to Köppen (1931) is also shown.See Appendix for detailed information on site location.