P.S.Z.N. I: Marine Ekology, LO (I): 79-94 (1989) 0 1989 Paul Parey Scientific Publishers, Berlin and Hamburg ISSN 0173-9565

Accepted: July 18.1988

Biogeography, Substrate Preference, and Feeding Types of North Adriatic I n t e rt i d a I Collembola

ERHARD CHRISTIAN

Institut fui- Allgcmeinc Biologic. Sehwarzspanicrstr. 17. A-1090 Vienna, Austria.

With 4 figiJrcs and 1 table

Kcy words: Collernbola, intcrtidal. biogeography, substrate prefcrcncc. lifc-form. mouthparts. gut contcnt.

Abstract. A survey OF North Adriatic intcrtidal Coflernholri is givcn. including thc tkst records of Fricseu ticrcminura. Archisorornu inrersririulis, Enrornobryu clollfrui. and Psrutlosinrllu Iiurcseri. Granulomctric and biococnological analyscs of culittoral loosc scdimcnts allowcd dctcrmination of thc animals' substratc prcfcrcncc. Thc limitation to cuhalinc habitats is tcstcd by comparison with mixohalinc shorcs nc:irby. Lifc-form typology is applied to clucidatc the largcly unknown rclations of intcrtidal Collcmbola to thc scdimcnt surfacc or supcrficial strata. Thc diffcrcnt modcs of nutrition arc distinguishcd by mouthparts and by gut contcnt analyses.

Problem

Apart from Acuri, Collembola are among the most frequent air breathing arthropods in roclky as well as in loose sediment shores. A great many springtail species from various systematic groups are known to be thalassophiles (seashore-dwellers by preference), and a few dozen thalassobiotic species are even limited to littoral habitats (STRENZKE, 1955; JOOSSE, 1976). In spite of their occasionally surprising abundance - up to 50,000 individuals per square meter can be found in salt marshes (WEIGMANN, 1973) - neither terrestrial nor marine ecologists have paid much attention to these intertidal apterygote insects. This contrasts with a series of physiological investigations, chiefly dealing with submergence resistance, problems of osmotic and ionic regulation, and the influence of salinity on life cycle parameters (WEIGMANN, 1973; WIITEVEEN & JOOSSE, 1987, 1988; WIITEVEEN et al., 1987). Tide-dependent activity patterns in littoral Coflembolu were reported by DAVENPORT as early as in 1903; the underlying endogenous rhythm was established for Anuridu maritimu (FOSTER & MORETON, 1981).

Abundant, albeit scattered autecological information, including feeding habits, dispersion, and life cycle, is only available for the largest and most

CHRISTIAN 80

conspicuous thalassobiotic springtail, Anurida maritima (IMMS, 1906; JOOSSE, 1966). VAN DER KRAAN (1975) reports o n the field-dependent distribution of the thalassophilous Hypogastrura viatica in a North Sea population. Collembolan communities of North Sea shores are described by ALTNER (1963) and WEIG- MANN (1973). Questions of habitat preference and niche segregation are studied in detail by SCHUSTER (1957, 1962, 1964). Valuable taxonomic, chorologic, and ecological data on North and Central American littoral springtails were recently published by CHRISTIANSEN & BELLINGER (1988).

Nevertheless, our knowledge of the geographic distribution of intertidal Collembola is still fragmentary. Among the European coasts, only the North Sea, the Baltic Sea, and the West Mediterranean are relatively well investi- gated. The records for the Adriatic shores, on the other hand, are sporadic (DENIS, 1933; SCHUSTER, 1962, 1964; POINSOT, 1971) except for Anurida maritima. Particularly the interstitial forms of loose sediment beaches have escaped notice.

Recent collections at thirty-one eulittoral stations with different substrates between the Island of Rab and the Lagoon of Venice provide an opportunity to complete the spotty distribution maps of certain coast-dwelling Collembola and to study the substrate preference especially of interstitial species. As no un- equivocal opinion about the feeding habits of marine springtails exists, the results of mouthpart studies and gut content analyses are presented here in order to establish functional trophic groups in addition to the conventional life- form typology.

Material and Methods

All collections werc carricd out betwcen July and September in 1957 and 1988. Semi-quantitative samples werc taken 50cm inland of the respective watcrlinc. In each case the substrate was washed in three pits, 1 m apart, dug down 20cm below the water table (cf. SCHEERPELTZ, 1926). Floating arthropods were picked up by hand over a period of 15 min; the water surface within the pits was subsequently sucked off with the aid of an aspirator to collect even the smallest species and juveniles. In addition, survey samples were taken from rocky substrates and from brackish-water shores. For granutometric analysis, substrate samples taken ncar these “Scheerpeltz pits” were screened in the laboratory. The grain-size grade larger than 20 mm was considered insignificant with regard to the pore space habitable for Coflembolu and therefore rejected.

For studying the mouthparts, crushed preparations of single heads were mounted in Marc Andre ’I1 medium (MASSOUD, 1967). Prior to gut content inspection the midguts were dissected to avoid contamination with extraintestinal material.

Sampling sites Stations 1-24: semi-quantitative samples; 25-31: survey samples.

1: PrviC island, south of cape Njivica, in well-rounded medium gravel. 2: PrviC island, near cape StraZica, medium gravel with some grit. 3: Island of Krk, BaSka, near public campground, assorted rockfall (sandstone), in unconsoli-

4: Near station 3, but gravel fraction more dominant. 5: Near station 3, gritty gravel. 6: 300m north of station 3; 20cm thick layer of coarse sand and fine gravel overlaying medium

7: Island of Krk, Stara BaSka, grain size distribution similar to station 2.

dated material between boulders.

gravel and pebble.

North Adriatic intertidal Coilembola 81 8: Island of Krk, Sveti Fusca; natural harbour, angular sediment underlain by red stony loam

9: Island of Krk, Glavotok; medium gravel and grit. (terra rossa).

10 Island of Krk, Soline bay; loamy sediment with fragmented mollusk shells, 50cm off a Starice

11: Near station 10; wet mud next to the border of the halophyte belt. 12: Near station 10; sand, gravel, and mollusk shells between boulders. 13: Island of Krk, C*iZiCi; medium gravel and sand. 14: Istria, Rovinj, ’v‘e9tar bay; badly rounded material above terra rossa-like sediment between

15: Istria, Rovinj, north shore of Limski channel; sandy mud with thin sapropel horizons

16: Near station 15; similar sediment, but underlain by dark soil, vegetation down to lm off the

17: Sistiana Mare northwest of Trieste; mixed grain-size material with scattered cobblestones on

18: Caorle, Valle vixchia; sand beach east of the Lagoon of Caorle without mass tourism and

19: Caorle; muddy shore of the lagoon near Castello di Brussa with dense reed vegetation.

20: Caorle, Porto di Falconera north of the lagoon; sand under Ulva wrack. Mixohalinc water

21: Venice, lagoon near Cavallino; muddy sand forming “terraces” a few millimeters in height. 22: Near station 21, but coarser material. 23: Venice, Punta Sabbioni; dark sandy detritus with mollusk shells under superficial limestone

24: Near station 23, but sediment organically less enriched. 25: Island of Rab, L,opar, under stones on muddy fine sand. 26: PrviC island, foot of a vertical rock wall I m behind station 1. 27: Island of Krk, cliff near cape Skuljica. between watcr level and the entrance of Skuljica cave. 28: Island of Krk, BaJka; rocky shorc near camp Bunculuka. in moist crcviccs. 29: Island of Krk, Soline bay. littoral rocks near Klimno. 30: Caorle, near starion 19, canal with Phragrnifes along the muddy bank, electric conductivity

31: Caorle, mouth oil river Livcnza; silty mud between the bank stabilization blocks, mixohaline

stand.

boulders.

overlaying terra rossa between rocks.

waterline.

top.

with thick wrack deposit. Mixohaline water (11 %O salinity).

Mixohaline wattx (electric conductivity: 1 2 0 0 ~ s . cm-I).

(14% salinity).

boulders; thin snpropcl layer in lOcm depth.

590 pS. cm-I.

water (2650pS. c:m-l).

Results

1. Biogeography

Table 1 gives a survey of all intertidal collembolan species known so far from the north coast of the Adriatic Sea, including characteristic species from mixohaline habitats near the shore. The often used term “cosmopolite” is avoided for species with a wide range of distribution because of our poor chorologic knowledge. From a biogeographic viewpoint, the following records are of special importance:

Paraxenylla u#?nifomis. This hypogastrurid species was originally described from Bakar near Rijeka without indication of the habitat. After littoral records from France, the Azores, the Black Sea (RUSEK, 1965), and South Australia, DA GAMA & DEHARVENG (1984) discerned Xenylla afiniformis STACH 1929 as halophilous and erected a monotypic genus, Haloxenylla. CHRISTIANSEN & BELLINCER (1988) report on North American records and place affiniformis

CHRISTIAN 82 Table 1. Intertidal Collembola known to date from the North Adriatic coast. Individual numbers are not given for survey samples. *: no record from euhaiine habitats; x: thalassoxenic; ph: thalassophilous; bt: thalassobiotic; eur: European; eur-atl: European Atlantic coasts; hol: holarctic; med: Mediterranean; pal: palaearctic; large: known from several continents: N: first record for North Adriatic shores.

Species Habitat Range of Stations prefer- distribu- (individuals) ence tion

Hypogastruridae:

(TULLBERG) 1872 Hypogastrura viatica Ph large -

Ceratophysella denticulata gr. ? ? 17(1); 23(10). * Xenylla maritima TULLBERG 1869 ph Pal 19 (6). Paraxenylla affiniformis bt large 5(1); lO(9); 13(1); 16(20); 22(5);

(SCHUSTER, 1962: Palu near Rovinj)

(STACH) 1929 23(9); 24(2); 25.

Neanuridae: Friesea acuminata (DENIS) 1925 bt med, 3(6); 8(1); 12(8); 13(2); 17(10);

Anurida moritima ( G U ~ R I N ) 1836 bt large l l ( l1 ) ; 14(6); 15(11); 17(2); 18(2);

* Anurida rullbergi (SCHiSrr) 1891 ph hol 30.

eur-at1.N 23 (30); 24 (2).

20(38); 21(126).

Onychiurzdae. Protaphorura armata gr. ? ? 8(1). * Onychiurus pseudostachianus x eur 31.

GISIN 1956

Isotomidae:

DELAMARE DEBOUITEVILLE 1954 Archisotoma interstitialis bt 1arge.N I 1 (4); 2 (4); 3 (2); 4 (5); 5 (102); 6 (40);

7(11); 9(83); lO(2); 12(3); 13(4); 14(1); 17(7); 19(14); 20(1); 22(6); 23(6).

Isotoma boneti Ph med 25.

Axelsonia littoralis (MONIEZ) 1890 bt large 12(5); 13(2); 14(18); 22(1); 29. DELAMARE DEBOUlTEVlLLE 1954

Entomobryidae: * Sinella coeca (SCH~TT) 1896 x large 31. Entomobrya dollfusi DENIS 1924 ph med, 26; 27; 28.

Pseudosinella hauseri eur-atl,N

bt med,N 8(2). DA GAMA 1973

Sminthurididae: * Sminthurides aquaticus X hol 19 (4) ; 30.

* Sminthurides mafmgreni X large 30. ( B O U R L ~ ) 1843

(TULLBERG) 1876

North Adriatic intertidal Collembola 83 within Puruxenylla because the type species of this genus, P. mangle MURPHY 1965 from Gambia, is a synonym of ufiniformis.

Since STACH’S lypeS are poorly preserved, the records from the Island of Krk, situated next to the locus classicus, verify the conspecifity of all the ufiniformis- material collected so far and demonstrate the large distribution area of this obviously thalassobiotic species.

Friesea acurniitata. The North Adriatic records extend the documented area to the east. The statement “Costa Rica” in SALMON (1964) is erroneous.

Archisotoma interstitialis. Probably the most widespread species of an exclusively coast-dwelling isotomid genus. A. interstitialis inhabits Mediterra- nean coasts, including the Sea of Marmara and the Black Sea (CHRISTIAN, unpubl.). A single North Sea record is based upon subadult specimens (FJELL- BERG, 1980). Nearctic records (California, Mexico, Bahamas, Cuba) are com- piled by CHRISTI:ANSEN & BELLINGER (1988). POINSOT (1972) synonymizes A. xuvieri CARDOSO 1966 from Mozambique with A. interstitialis.

Entomobrya (Mesentotoma) dollfusi. This surface-dwelling littoral species, known from Irish, English, French, and Algerian shores, is occasionally found some kilometers inland (CHRISTIANSEN, 1956; BOLGER, 1986). The documented North Mediterranean area is now considerably expanded to the east.

Pseudosinella hauseri. After the original description from a seashore station of the Island of L.evkas this entomobryid species has not been reported again. The Adriatic animals agree in all body characters with a single specimen from Corsica (Sant Amara near Bonifacio, leg. E. CHRISTIAN, 7.7.1986) which was collected in littoral fine gravel. Ps.haureri may therefore turn out to be a widespread Mediterranean seashore-dweller.

If those species collected only at mixohaline stations are disregarded, a total of eleven eulittoral Coflembofu are known from the North Adriatic. Two of them cannot be determined reliably, five are distributed over a wide area and are known from the coasts of at least two continents, two inhabit Mediterranean and European Allantic coasts, and two are possibly limited to the Mediterra- nean. Exclusively Adriatic species have not been found.

2. Substrate preference and ecological potency

Size and arrangement of interconnecting substrate pores are among the deter- minants of the micro-distribution of soil-dwelling and interstitial Collembolu. Since springtails are hardly able to widen given cavities, they are dependent on a suitable pore architecture; this can clearly be demonstrated for the coenoses of virgin sandy soils (CHRISTIAN 8c THIBAUD, 1988). CONRAD (1976) ascertained experimentally that Anuridu rnaritirnu is more abundant in an angular sand substrate than in rounded sand of the same grain size. Therefore, grain-size distribution in littoral substrates might influence the composition of collembolan communities. A high amount of fine material should exclude the larger intersti- tial forms, while other species could be handicapped in coarser substrate, either by unfavourable nutritional conditions, by increased competition, or simply by being washed out. To test this, the dominance graphs of 24 semi-quantitative samples are related to the respective (rounded) granulometric results in Fig. 1.

84 CHRISTIAN

0.2-2.0 mm Fig. 1. Grain-size distribution and dominance spectra of the collembolan fauna at 24 semi-quantita- tively sampled stations.

The triangle diagram confirms the above hypothesis. Archisotoma interstitialis proves to be the least substrate-specific of all interstitial forms encountered. It occurs even in pure gravel where no other Collembola can be found. On the other hand, A. inferstifialir inhabits sandy and silty-sandy shores as well, although with reduced dominance.

Friesea acuminafa and Axelsonia littoralis prefer granulometrically mixed substrates, being absent in fine-grained material and in pure gravel. While F. acuminafa is an interstitial species, A. littoralis has frequently been reported from rocky shores. An ecological connection of the latter species with solid rock habitats is indicated by the fact that all Axelsonia-stations investigated in this study neighbour corroded rocks or boulders. As A. littoralis avoids rocky cliffs

North Adriatic interticlal Collembolu 85

without any clastic sediment, a structurally diversified habitat Seems essential for its distribution. This conclusion is corroborated by its regular Occurrence in the pore space of the Mediterranean Lithophyllum tortuosum trottoir (SCHU- STER, 1957, 1962).

For Entomobryo dollfusi, on the other hand, a surface-near pore system is not necessary. Living ia mainly epigeal life, this entomobryid species (not included in Fig. 1) is able to ccllonize the spray zone of cliffs free of loose’material. Although sometimes rather abundant at the foot of vertical rock walls (e. g., station 25), E. dolrfusi does not penetrate into the subjacent sediment layer.

Paraxenylla affiniformis covers a wide range of substrate types, but shows highest abundance and dominance in fine-grained and muddy material, pro- vided that a mesh-work of interconnecting pores is guaranteed by a frame of larger mineral particles or fragmented mollusk shells.

Anurida maritinza dominates fine-grained substrates in spite of its large body size, but all of the: Anurida-stations are characterized by superficial structures which provide the animals with shelter at high tide: station 11 is a salt marsh with dense halophyte vegetation, stations 18 and 20 are situated on sandy beaches with wrack deposits, and at the other stations fissured rocks in close vicinity serve the same purpose. Thus, in the North Adriatic, A. maritirna proves to be restricted to coasts with sufficient spatial structures to allow retreat. This agrees well with JOOSSE’S (1966) description of “nests” around the roots of plants where the animals are congregated and enclosed in an air bubble during high tide. According to the same author, A. maritima has not yet been recorded from sandy beaches in The Netherlands. Burrowing behaviour in sandy sub- strate as reported by DAVENPORT (1903) and IMMS (1906) cannot be confirmed for the Adriatic populations.

The coenologic comparison with littoral habitats at reduced salinities allows a conservative appraisal of the ecological potency of some species. Anurida maritima, unable to survive freshwater conditions, has a physiological optimum at normal seawater salinity (WIT~EVEEN & JOOSSE, 1987). At station 18, A. maritirna was found at a salinity of 11 %. As the water freshens further (station 29), this species is replaced by the thalassophilous Anuridu rullbergi which, in turn, does not inhabit euhaline shores in the area under consideration. In view of the physiological stenopotency and the observed distribution, A. muritima is considered to be thalassobiotic in spite of a few reliable inland records (STACH, 1949; DA GAMA, 1964) - unless permanent inland populations can be proven.

The occurrence of the doubtlessly thalassobiotic Archisotoma interstitialis at the mixohaline station 19 is fairly surprising and indicates a broad osmotoler- ance. The factors limiting this species to moist habitats near the seashore remain unknown.

Onychiurm pseudostachianus is no “marine” collembolan at all, but rather characteristic of wetlands and “abbondantissimo nella marcita lombarda” (DAL- LAI, 1969). The record at the mouth of the river Livenza proves its ability to cope with varying !salinities.

86 CHRISTIAN

3. Life-forms

Applying the widely accepted life-form typology to Adriatic intertidal Coffem- bola, one can distinguish two major groups: hemiedaphic (Fig. 2 a-d) and epedaphic (Fig. 2 f) life-forms. While the hemiedaphic forms are characterized by a bulky shape, short appendages, short or missing furca, uniform and frequently reduced pigmentation, and often a numerical reduction of ommatidia, the epedaphic ones exhibit the opposite features. In the case of North Adriatic intertidal springtails, this rough classification agrees well with the animals’ life habits. The only exclusively surface-dwelling species, Entomo- brya dollfusi, represents the epedaphic life-form in a most exemplary way, while Axefsonia lirroralis (Fig.2e), a species which inhabits both the surface and interstitial strata, shows an intermediate habitus. In hemiedaphic and predomi- nantly interstitial species (Paraxenylla affiniformis, Friesea acuminata, Archisotoma intersritialis), the body pigment is comparatively well developed, indicating at least episodic exposure to sunlight. Accordingly, Anurida maririma, a regular visitor of the surface, is completely black. No morphological adaptations to an epineustic mode of life, such as the buoy-like inflation of the mucro in Sminthurides aquaticus and Sm. rnalmgreni, are evident in the interti- dal species.

Fig. 2. Habitus and life-form of North Adriatic intertidal Collembola. (a) Anuridu rnuritimu, body length (without appendages) up to 3.0mm. (b) Friesea acuminata, 1.5 mm. (c) Paruxenylla ufjinifor- mL. 0.9mm. (d) Archiroioma interstitidis, 1.2 mm. (e) Axelsonia li(toraIis, 2.0mm. ( f ) Eniomobrya dollfusi, 2.2 mm.

87 Forms of eueldaphic habitus like the widespread thalassobiotic Anuridella

North Adriatic intertidal Collembolu

calcarata DENIS 1925 were not found in the Adriatic material.

4. Mouthparts and food

The plesiomorphic state of the entognathous collembolan mouthparts is biting- chewing, being present in the majority of the taxa. Among the marine species compiled in Fig. 1 , Axelsonia littoralis (Fig. 3 a) and Entomobrya dolrfusi are equipped with buccal extremities of this type. The mandible bears strong incisor teeth and a large molar plate; the maxilla head or lacinia shows a main shaft (ungulum) with well-developed blunt apical teeth and elastic lamellae. As the gut content analyses suggest, A . littoralis (Fig. 4 a) and E. dollfusi collect parti- cles from the submjtrate and rasp the surface of grains and rocks; this results in a high amount of mineral matter. No animal material could be identified within their guts.

Archisotoma irzterstitialis (Fig. 3 b) and Paraxenylla affiniformis (Fig. 3 c) re- present an as yet functionally unexplained configuration of modified mouth- parts. The incisor part of the mandible is small and placed on top of a long “neck” which separates it from the molar part. The hard structures of the lacinia are reduced to a single rod-like ungular process (black in Fig. 3 b, c), while the soft, fringed lamellae make the maxilla head look like a feather duster. This unusual configuration indicates a sweeping or wiping function of the maxilla and hence a detritivorous nutrition. This hypothesis is supported by the similar results of the gut content inspections in both species (Fig. 4 b): the ingested material consists (of compactly bedded small particles of predominantly organis- mic provenance. There are neither indications of a shredding or crunching mouthpart-action nor is there any hint at selective food-particle collection. A. interstitiafk an’d P. affiniformis are obviously small-particle feeders, living on organic detritus i n an advanced state of mechanical and probably also biogenic reworking; they mop up the fine-grained sediment chiefly with the aid of their extraordinary maxilla heads.

Another deriv’ed type of mouthparts, termed biting-sucking, is present in Anurida rnaritimu and Friesea acuminata (Fig. 3 d, e). The mandibular as well as the maxillary incisors are strong and pointed; the molar plate is completely missing and the lamellae of the maxilla head are reduced in number. A . maritima was observed by several authors to often feed on dead or moribund animals. The guf content analyses confirm a preferential animal diet of this species. Fifty transparentized specimens from different sampling sites with visible gut contents were dissected, but identifiable particles were found in only nine guts. In seven cases, crustacean remains were determined (Fig. 4c), in one the remains of Archisotoma interstitialis, and in the last a few diatom shells. In all guts a homogeneous matrix with very few mineral grains was visible - most probably maceraced animal tissue or sucked-up body fluid.

The gut content of Friesea acuminata is similar, but remains of the collembo- lan Archisotoma interstitialis within the unstructured matrix prevail by far. In Fig. 4 d two maxilla heads of A . interstitialis are discernible. Six of seven guts

88 CHRISTIAN

Fig. 3. Mouthparts of intertidal Collembola. Left: mandible; Right: maxilla head. (a) Axelsonia littoralis. (b) Archisotoma interstitialis. ( c ) Paraxenylla afiniformis. (d) Anurida maritima. (e) Friesea acuminata.

with determinable structures inside (out of 16 investigated specimens with filled guts) contained Archisotoma extremities; in only one case was non-collembolan arthropod cuticle detected. These collembolan remains were not exuviae: in three guts, muscle fibres were still attached to springtail limbs. There is little doubt that F. ucuminutu is predaceous on other littoral Collembolu.

Piercing-sucking species with stylet-shaped mouthparts are absent in the investigated habitats. This nutritional type, as classically represented by the subfamily Neunurinae, is widespread and rather frequent in many terrestrial biotopes, but quite uncommon among intertidal Collembolu.

North Adriatic intertidal Collernbolu 89

Discussion

The North Adriatic shores prove to be almost as rich in thalassobiotic intertidal collembolan species as are the well-investigated West Mediterranean coasts. In fact, there is a high degree of faunological conformity due to the generally wide distributions of eulittoral springtails. The absence of the genus Anurideflu on Adriatic shores may reflect ignorance more than true biogeographic differences, especially since A. cufcurufu, known from North American and European Atlantic coasts and from the West Mediterranean, was recently recorded from the south coast of the Sea of Marmara (Yenikoy near Karacabey, leg. K. WITT- MANN, 6.7.1988).

CHRISTIAN 90

Fig. 4. Gut content of intcrtidal Collembola. Bar length: 50prn. (a) A.reluoniu liiiordis. (11) Paraxenyilu ufjniformis. (c) Anurida muriiima. (d) Frieseu acurninura.

Since most littoral Collembofu temporarily or permanently inhabit substrate pores, a grain-size influenced dispersion should be expected. The environmental conditions within the pores of gravelly sediments obviously match the demands only of Archisotoma inrerstitiafis, the most eurypotent species with respect to granulometric composition. A. interstirialis is one of the smallest intertidal springtails, which makes a direct effect of pore space unlikely. Much autecologi- cal information remains to be gathered before the factors preventing other Collembola from colonizing gravel deposits of the intertidal zone can be determined. Granulometrically mixed substrates, as represented in the centre of the triangle diagram (Fig. l ) , can be settled by all of the thalassobiotic species, while species numbers decrease markedly towards the corners of the diagram (the mixohaline station 19, grown over with reed, should be ignored in this connection). This suggests a notable influence of structural sediment diversity on species diversity.

Specialized and morphologically adapted sand-dwelling Coffembola are absent from the North Adriatic intertidal zone. In supralittoral dunes, however, this euedaphic-interstitial life-form is quite common (THIBAUD & CHRISTIAN, in press). The fact that all intertidal species encountered represent hemiedaphic life-forms indicates a weak tie to subsurface habitats or, more precisely, periodical or at least episodical surface stays. Whether such vertical migrations are as regular as in Anurida rnaririma in all cases (FOSTER & MORETON, 1981) remains open, but the mechanical instability of sediments in the zone of wave action could explain the hemiedaphic life-form type of even the smallest species.

Different reactions of closely related species with respect to salt concentration are most clearly demonstrated by the two Anurida species. A . tullbergi, often referred to as thalassophilous or halophilous, does not colonize coasts of normal

North Adriatic intertidal Collembolu 91 marine salinity in the North Adriatic region. DELAMARE-DEBOUTEVILLE (1955) points out that this species avoids contact with salt water, although it is frequently found on continental halomorphic soils. In the coastal environment, A. tullbergi prefers supralittoral habitats and may only occasionally be washed to the intertidal zone. A . maritima, on the other hand, lives at the mesomixo- haline station 18 (11 %o salinity). This is probably near the lower border of its salt tolerance, considering the osmoconform reaction of its haemolymph due to a total loss of hyper-regulation ability (WITEVEEN et al., 1987).

The record of ,4rchisotoma interstitialis at station 19 again proves the eurypo- tency of this marine springtail; it turns out to be not only the least substrate- specific but also the most osmotolerant among the thalassobionts under con- sideration.

A striking feature of the thalassobiotic collembolan fauna is the high percen- tage of species with modified mouthparts. Along North Adriatic shores, only Axelsonia littorar’is and Pseudosinella hauseri belong to the original biting- chewing type, the most frequent one in almost all terrestrial coenoses.

Friesea acuminufa and Anurida rnaritima, both equipped with biting-sucking mouthparts, feed on animals. This corroborates the observation that predacious or necrophagous collembolan species are proportionally more numerous in littoral communities than in normal soils (CHRISTIANSEN, 1964). Friesea species are apparently carnivorous irrespective of habitat. Nonetheless, a collembolan like F. acuminatfi; feeding mainly upon another springtail species, is a rare exception. MACNAMARA (1924) reports on Metisotoma grandiceps (REUTER) 1891 devouring the North American snow springtail Hypogastrura nivicoln (FITCH) 1846, but CHRISTIANSEN & BELLINGER (1980) refer to this isotomid as “probably not exclusively carnivorous”. All other casual observations of spring- tail-eating Collembola indicate a rich menu. Collections along other Mediterra- nean coasts are necessary to determine whether F.acuminata is a springtail- eater by preference or rather an opportunistic carnivore like Anurida maritima. This latter species is known to feed upon a variety of animal remains ranging from dead fish to mollusks. An occasional uptake of algae was first observed by IMMS (1906). The: predominance of crustacean remains in the guts of Adriatic animals is probably due to accidental food availability rather than being proof of regional stenophagy. CHRISTIANSEN & BELLINGER (1988) found annelid remains in the guts of North American intertidal Anuridu and Friesea species.

The “wiping” mouthparts of Paruxenylla affiniformis and Archisotoma inter- stitiafis are convergent formations which are not restricted to seashore-dwellers, but are evidently more frequent in species from wet habitats. A functionally similar shape of the mouthparts is found, for instance, in the onychiurid Ussuriaphorura pluripseudocellata MARTYNOVA 1979 and in the isotomid Gnathofolsomia palpafa DEHARVENG & CHRISTIAN 1984, a cavernicolous spring- tail living on hygropetric rocks. The results of ENGHOFF (1985), who describes a comparable mouthpart modification in several unrelated cave-dwelling mil- lipedes, are of special interest in this connection. All diplopod species with reduced biting-chewing mandibular parts and hypertrophied feathering lamellae live in contact with subterranean water; this leads ENGHOFF to conclude a screening function of these structures. The high frequency of “wiping” Collem-

CHRISTIAN 92

bola in coastal habitats supports the idea of a functional relation between wet environment and plumose mouthpart lamellae. In thalassobiotic Collembola, however, there is no indication of a true filtering of suspended organic material.

Summary

1) Eleven collembolan species are now known from the intertidal zone of the North Adriatic coast; six are considered thalassobiotic. Adriatic endemics are missing. 2) The granulometric composition of the substrate influences the dispersion of seashore Collembola. In pure gravel only Archisotoma interstitialis can exist. 3) Anurida maririma, although physiologically adapted to euhaline water, can tolerate mesomixohaline conditions. 4) Euedaphic life-forms and morphologically adapted sand-dwellers are not present in the intertidal zone. 5) Among the thalassobiotic Collembola, only Axelsonia littoralis and Pseudosinella hauseri are equipped with the plesiomorphic biting-chewing mouthparts. The biting-sucking type is represented by the predominantly car- nivorous Anurida maritima and Friesea acuminata. The latter was shown to feed upon Archisotoma interstitialis. Paraxenylla affiniformis and Archisotoma inter- stitialis “wipe” small particles with the aid of their feathery maxilla head lamellae.

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