are Chirocephalus diaphanus, Branchipus schaefferi and Tanymastix stagnalis (Figures 1â2). They build large populations in waterbodies of different kinds.
Hydrobiologia 405: 57–65, 1999. © 1999 Kluwer Academic Publishers. Printed in the Netherlands.
57
Current status of the Anostraca of Italy Graziella Mura Dipartimento di Biologia Animale e dell’Uomo, viale dell’Universit`a 32, 00185 Roma, Italy Received 2 November 1998; in revised form 27 April 1999; accepted 20 May 1999
Key words: Anostraca, Italy, IUCN evaluation
Abstract Fairy shrimp distribution in Italy is updated on the basis of recent records . Their status is evaluated according to IUCN Red List criteria in order to document the current situation and to rectify previous incorrect assessments. Most of the 16 species have at least one population in a protected area, so that they apparently face little risk. Only Branchipus pasai and B. blanchardi are potentially threatened by future habitat alteration. It is stressed that data on fairy shrimp distribution are far from complete and limited to certain regions of the country. Their range reflects the specialist distribution and ‘migratory activity’ rather than that of the animals themselves.
Introduction Systematic investigations on Anostraca in Italy started during the 1960s (Ruffo & Vesentini, 1957; Stefani, 1961; Stella, 1963; Stella et al., 1967; Cottarelli, 1967, 1968a, b; Cottiglia & Tagliasacchi-Masala, 1968; Stella & Margaritora,1968; TagliasacchiMasala, 1969), though first contributions date back to the 1930s (Colosi, 1922; Masi, 1925; Artom, 1927). The regions surveyed were Latium (central Italy) and Sardinia, actively explored also during the 1970s (Stefani, 1971; Cottarelli & Mura, 1973, 1975; Margaritora et al., 1973; Stella & Margaritora, 1975; Serra, 1977). Since then, investigations were extended to other regions, though at a lesser extent (Cottarelli & Mura, 1984; Mura & Barsotti, 1985; Cottarelli et al., 1995). The most recent records include the discovery of Streptocephalus torvicornis in San Nicola, Tremiti Islands (Mura & Cottarelli, 1998) and of Branchinella spinosa in Apulia (Mura et al., in press). To date 16 species have been recorded: Artemia parthenogenetica Bowen & Sterling, 1978; Artemia salina Linnaeus, 1758; Branchinella spinosa MilneEdwards, 1840; Branchipus blanchardi Daday, 1908 (syn. B. alpinus Colosi, 1922); B. pasai Cottarelli, 1968; B. schaefferi Fischer, 1834; B. visnyai Kertesz, 1956; Chirocephalus diaphanus Prévost, 1803; C.
kerkyrensis Pesta, 1936; C. marchesonii Ruffo & Vesentini, 1957; C. ruffoi Cottarelli & Mura, 1984; C. salinus Daday, 1910; C. sibyllae Cottarelli & Mura, 1975; Streptocephalus torvicornis Waga, 1842; Tanymastix stagnalis Linnaeus, 1758; T. stellae Cottarelli, 1967. Although large parts of the country remain unexplored, a tentative analysis of the distribution and conservation status of species is presented in this paper. Methods and materials Specimens were collected over the last 40 years (1958–1998) by both private and university expeditions. Samples fixed in formaldehyde 4% or ethanol 80% are stored in the collection of the Department, Faculty of Sciences, Rome La Sapienza. Many of the sampling sites, especially in threatened areas, are periodically revisited. Results Status of the species and their habitats in Italy Of the species listed in Table 1, the most widespread
58 Table 1. The italian anostracan fauna indicating IUCN Red List category (1996) Species
ARTEMIA A. parthenogenetica Bowen e Sterling, 1978 A. salina Linneus, 1758 BRANCHINELLA B. spinosa Milne-Edwards, 1840 BRANCHIPUS B. blanchardi Daday, 1908 B. pasai Cottarelli, 1968 B. schaefferi Fischer, 1834 B. visnyai Kert´esz, 1956 CHIROCEPHALUS C. diaphanus Pr´evost, 1803 C. kerkyrensis Pesta, 1936 C. marchesonii Ruffo e Vesentini, 1957 C. ruffoi Cottarelli e Mura, 1984 C. salinus Daday, 1910 C. sibyllae Cottarelli e Mura, 1975 STREPTOCEPHALUS S. torvicornis Waga, 1842 TANYMASTIX T. stagnalis Linneus, 1758 T. stellae Cottarelli, 1967
IUCN Red List
Number of localities
Status within pools
Number of conserved areas
Distribution in Italy
Endemic to Italy
Last year of collection
N
1997
N
1997
LR lc
4
C
1
LR lc
8
C
2
Emilia-Romagna, Apulia, Sardinia Latium, Sardinia
VU B1+ 2c,d
7
C
2
Apulia, Sardinia
N
1998
VU D2
2
C
–
Piemonte
N
1996
VU D2
5
C
–
Is. Lampedusa (Sicily)
N
1997
13
C
3
N
1997
1
C
–
Latium, Abrutium, Apulia, Sardinia, Sicily Latium
N
1997
LR lc
29
C
5
N
1998
LR cd
5
C
2
Piemonte, Umbria, Latium, Abrutium, Campania, Apulia, Sicily Latium
N
1998
LR cd
1
C
1
Marche
Y
1998
LR cd
2
C
2
Emilia-Romagna, Basilicata
Y
1998
13
C
2
Sardinia
N
1997
LR cd
1
C
1
Marche
Y
1997
LR cd
1
U
1
Apulia
N
1993
LR lc
12
C
4
N
1998
1
–
–
Tuscany, Umbria, Latium, Abrutium, Sardinia Sardinia
N
1970?
LR lc VU D2
VU B 2c,d
EX
LR(lc)=Lower risk, least concern; VU=Vulnerable; EN=Endangered; CR=Critically Endangered; status within pools (Common (C)=more than 20 specimens collected from at least one pool; Uncommon (U)=between 6 and 20 specimens collected from at least one pool; the number of localities from which the species has been collected; whether the species occurs in a formal conservation area (Y=yes; N=no) and the year that the species was last collected.
59
Figure 1. Distribution of Chirocephalus species (shaded areas indicate national or regional parks, reserves or oasis).
are Chirocephalus diaphanus, Branchipus schaefferi and Tanymastix stagnalis (Figures 1–2). They build large populations in waterbodies of different kinds (from small puddles to large ponds). C. diaphanus is undoubtedly the most tolerant species, occurring in any freshwater type, in lowlands or in mountains and even in permanent lakes and ponds (for example, Lake Tilia in the Appennino Reatino, central Italy or Castelporziano Presidential Estate, Rome). It sometimes associates with Chirocephalus kerkyrensis (Castelporziano), Branchipus schaefferi (coastal pools in Pian di Spille, Tarquinia, Latium), or Tanymastix stagnalis (Pantani di Forca Canapine, Appennino Reatino, Latium). Branchipus schaefferi prefers ponds with loamy sediment and turbid water with no or sparse vegeta-
tion(Hössler et al., 1995; Petkowski, 1997; Petrov & Petrov, 1997). In Italy it is most frequent in mountain pools above 1500 m. a.s.l., but we also have records from coastal rock pools on the island of Favignana (Trapani, Sicily), in Apulia, (south-eastern Italy) and from a ricefield in Sardinia (Oristano). Unlike in Austria ( Hössler et al., 1995), it seems absent from permanent waters. Tanymastix stagnalis too seems restricted to temporary waters and commonly occurs in small rock pools of limited depth, with clear water, no vegetation or with grass and moss at the bottom. These are located in Sardinia (north-eastern coast, La Maddalena Archipelago, Caprera) and in the Tuscan Archipelago, where the species occurs at or close to sea level, as in other parts of its home-range (Maier & Tessenow,
60
Figure 2. Distribution of Branchipus, Tanymastix and Streptocephalus species (shaded areas indicate national or regional parks, reserves or oasis).
1983; Freiner & Grüttner, 1984; Petkowski, 1995; Eder et al., 1997). The species may also be found in larger pools (Grainger, 1991), sometimes with turbid waters, at high elevations (for example Pantani di Forca Canapine and Fosso dei Mergani, Appennino Reatino, Latium, central Italy). Populations never become extremely dense, in any habitat. In contrast with C. diaphanus and B. schaefferi, T. stagnalis seems intolerant of high temperatures (Mura, unpublished observations); in spite of this and of the low optimum documented in the literature (Grainger, 1981; Maier & Tessenow, 1983; Freiner & Grüttner, 1984), it cannot be classified as cold stenothermal (Müller, 1918; Flössner, 1972), since it often occurs at water temperatures of 25–30 ◦ C, e.g. in Austria (Eder
et al., 1997). When co-occurring with B. schaefferi, T. stagnalis is the first to appear after snowmelt and it is the first to disappear with increasing temperature. It has to be noted, however, that it is the pattern of variation (Mura, 1997) that affects life cycle more than temperature itself. The second Tanymastix species, formerly occurring in Sardinia, was known only from its type locality, two rock pools in Orosei (south-eastern coast), eliminated by urbanization. Other anostracan species recorded in a relatively high number of localities (Table 1) are: Chirocephalus salinus, Branchinella spinosa, Artemia salina and A. parthenogenetica.
61 Table 2. List of protected areas in Italy including anostracan habitats Name
Year of Occuring Institution species
Parco Nazionale Abruzzo (Central Italy) Parco Nazionale del Circeo (Central Italy) Tenuta Presidenziale di Castelporziano (Central Italy) Oasi LIPU Zona Umida di Sale Porcus (Sardinia) Riserva Naturale Statale Salina di Tarquinia (Central Italy) Parco Regionale Alto Appennino Modenese (Northern Italy) Parco Regionale Appia Antica (Central Italy) Parco Naturale Regionale Delta del Po’ (Northern Italy) Parco Nazionale Arcipelago Toscano (Central Italy) Riserva Marina Isole Egadi (Sicily) Parco Nazionale del Pollino (Southern Italy) Parco Nazionale del Gargano (Southern Italy) Parco Nazionale del Gran Sasso e dei Monti della Laga (Central Italy) Parco Nazionale dei Monti Sibillini (Central Italy)
1923
Chirocephalus diaphanus
1934
Chirocephalus kerkyrensis
1972
Chirocephalus diaphanus Chirocephalus kerkyrensis
1976 1982
Branchinella spinosa Artemia salina
1980
Artemia salina
1988
Chirocephalus ruffoi
1988
Chirocephalus diaphanus
1988
Artemia parthenogenetica
1989
Tanymastix stagnalis
1989
Branchipus schaefferi
1990
Chirocephalus ruffoi
1991
Branchipus schaefferi Streptocephalus torvicornis
1993
Chirocephalus diaphanus Branchipus schaefferi Tanymastix stagnalis
1993
Chirocephalus marchesonii Chirocephalus sibyllae Tanymastix stagnalis Chirocephalus diaphanus Chirocephalus salinus Branchinella spinosa
Riserva Nazionale Marina Isola di Mal di Ventre e Sinis (Sardinia) Oasi della Giara di Gesturi (Sardinia)
1998
proposed Chirocephalus salinus
The first is confined to Sardinia and sardinian islands and occurs from ditches along the road in the northern area, to large ponds with clear or turbid water. It occurs also in a series of large rock pools on the basaltic plateau Giara di Gesturi (Cagliari, south Sardinia). Only two of the 13 localities known for this species (Tables 1, 2) are protected and most of the others are threatened by human activities. Branchinella spinosa, thriving in waters rich in chlorides and sulphates, is not confined to Sardinia as previously supposed, but was recently found in a pond along the Ionian coast of Apulia (south-eastern Italy). There, it co-occurs with Artemia parthenogenetica (Mura et al., in press). Its pools have a uniform appearance and are characterized by a large surface area, limited depth and marked astatism. Of Artemia, the bisexual species is typical of the Tyrrhenian coast, being widespread particularly in Sardinia (Figure 3), whereas the parthenogenetic one occurs along the Adriatic coast. Both thrive in man-managed or abandoned saltworks, more rarely in coastal ponds (Mura, 1987). Anostracans with more restricted distribution include Chirocephalus kerkyrensis and Branchipus pasai. The first one, confined to Mediterranean plain forest (Mura, 1997),in Latium and Corfù (Greece), formerly occurred in a great number of localities but is now restricted to few sites in the provinces of Rome and Latina. It is a winter form living in small pools as well as in large flooded areas of the mixed wood named ‘Piscine’ (e.g. in Castelporziano and in Circeo National Park), unable to survive rapid temperature changes. Branchipus pasai, also known from North Africa, occurs on the Island of Lampedusa (Sicily), where it has been recorded in five localities, few kilometers apart (Cottarelli, 1968a). It typically lives in small rock pools with a very short flooding, due to low rainfall of the area (less than 400 mm y−1 ). Branchipus blanchardi (synonimized with B. alpinus Colosi by Alonso, 1989) is restricted to the High Alps of France and Italy (Brtek & Thiéry, 1997). It lives in only two sites (at 1800 m. a.s.l.) of the province of Cuneo (Piemonte, north Italy): Lago Bagnour and Lago Secco. Both are small, shallow alpine lakes with transparent waters without emerging vegetation. Near Lago Bagnour, B. blanchardi was also found in few temporary pools. Two localities are known for Chirocephalus ruffoi, one of the three endemics of Italy. Both are located high in the mountains; the type locality is situated in
62
Figure 3. Distribution of Artemia and Branchinella species (shaded areas indicate national or regional parks, reserves or oasis).
southern Italy (a series of four pools at 1780–1900 m. a.s.l. in Piani di Pollino, Pollino National Park) (Cottarelli & Mura, 1984). The second locality (Rebecchi et al., 1990), are two pools at 1776–1778 m. a.s.l. in Monte Rondinaio, Appennino Modenese, northern Italy). All are characterized by small area and shallow depth and a loamy bottom without vegetation or with grass. The four remaining species, Chirocephalus marchesonii, C. sibyllae, Branchipus visnyai and Streptocephalus torvicornis are known from one locality each, although S. torvicornis was seen in a few puddles. Chirocephalus marchesonii and C. sibyllae occur in the Appennino Umbro-Marchigiano (central Italy), at 1948 m. and 1700 m. a.s.l., respectively; the first
lives in the permanent oligotrophic lake of Pilato, where it appears at the beginning of summer (Mura, 1993b). The second occupies a large pasture pool in Monte Palazzo Borghese (Mura & Calzecchi-Onesti, 1983). Both sites are part of the National Park of Monti Sibillini. Branchipus visnyai lives in a large astatic pond with muddy bottom and in a small temporary pool with grassy bottom close to the pond (Mura, 1996). Filling and duration of the pool is erratic. In the pond, two generations may appear: one at snowmelt, the other in autumn, depending on summer rainfall. In my experience, this pattern is common in temporary mountain waters, but occurs in some plain pools as well. Consequently, depending on climatic pattern and on ecological requirements of a species, several gen-
63 erations may appear within a season, as in the case of the Serbian populations of Branchipus schaefferi and Chirocephalus diaphanus carinatus (Petrov & Petrov, 1997). Streptocephalus torvicornis was recorded first in 1992 in San Nicola (Tremiti Islands, Apulia). This is considered to be a consequence of the climate variation characterizing the area (Mura & Cottarelli, 1998). Birds migrating from the Balkans across the Adriatic Sea, stopping on these Islands to rest and feed might have imported the species from eastern Europe and its occurrence totally depends on variations in annual weather. Infraspecific identification revealed that the specimens from Apulia show the features of the taxon from east Europe and should be assigned to the subspecies S. torvicornis torvicornis.
Discussion As in most of the world, ephemeral aquatic systems in Italy are threatened by human activities. Disturbances of pools are mostly linked to expanding urban and agricultural use; however, energy exploration and production, recreation and stocking with fish, may also cause important impacts. Like in many other instances (Bratton & Fryer,1990; Eng et al., 1990; Löffler, 1993; Petrov & Petrov, 1997), uncounted numbers of biotopes and their populations have thereby been eliminated, often without knowledge of what species existed there. A classical example in Italy is the extinction of Tanymastix stellae in Sardinia. Many similar cases may have occurred either on the Islands or on Peninsula, resulting in a decrease in the number of localities for most species. Among others, in Sardinia, one of the largest Branchinella spinosa populations was eliminated by the transformation of Simbirizzi pond, (Cagliari province) into a freshwater reservoir; similarly, many of the Chirocephalus diaphanus and kerkyrensis populations in Latium disappeared because of expanding urbanization. Obviously, the rarer the species, the heavier the consequences of human impact. Fortunately, the endemic species are located in isolated areas at high elevations, so that they are not directly endangered and are safe in these areas included in National Parks. Thanks to an improvement in preservation policy since the 1980s, an increasing number of valuable temporary water bodies have been
protected, so that the situation seems presently less critical. The pattern summarized in Tables 1 and 2, reveals that most of the 15 species presently existing in Italy have at least one population in a protected Reserve or a Park; these should be classified as Low Risk according to IUCN criteria, while a different evaluation has to be made outside of such areas (Table 1). Branchipus blanchardi and B. pasai are found in unprotected, restricted, isolated areas. They are hence potentially threatened, and are therefore evaluated as vulnerable. Unfortunately, due to lack of adequate control of protected areas, conflicts of interests with local human populations and, last but not least, people’s ignorance, sometimes even pools in protected areas may be threatened. As an example I mention uncontrolled collecting by tourists (like was the case for C. marchesonii in 1990), or bottom compaction by cattle using the pools to drink. According to Grainger (1991), this possibly resulted in the elimination of Tanymastix stagnalis from a number of pools in Ireland. The pattern here described is nonetheless far from conclusive due to gaps existing in the coverage on the territory. As previously noted (Dumont et al., 1995) “the known ranges of certain less charismatic animal species, generally reflect the distribution of their experts, in many instances few”. From Figures 1–3, it is evident that the apparent distribution of Italian anostracans confirms Dumont’s assertion, the data being concentrated in Latium and nearby areas. The recent discovery of Branchinella spinosa or of Streptocephalus torvicornis torvicornis in Apulia illustrates the problem of inadequate sampling to knowing the status of species. In this respect, caution should also be applied to species identification from cysts collected in the mud. For example, Tanymastix stellae was stated to occur in Corsica on such evidence (Thiéry & Gasc, 1991), but the cysts of all species of this genus are absolutely indistinguishable from each another. The present evaluation using the IUCN criteria (1996), widens and rectifies the limited and incorrect information available in the first National Red Data Book in which anostraca were included (Groppali & Priano, 1992), but still covers a restricted number of regions. For this reason it remains unsatisfactory and in need of expanding.
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