TAXONOMICAL SIGNIFICANCE OF SCANNING ELECTRON MICROSCOPIC MORPHOLOGY OF THE EUPHYLLOPODS’ RESTING EGGS FROM MOROCCO Part I. Graziella Mura, Alain Thiery

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Graziella Mura, Alain Thiery. TAXONOMICAL SIGNIFICANCE OF SCANNING ELECTRON MI- CROSCOPIC MORPHOLOGY OF THE EUPHYLLOPODS’ RESTING EGGS FROM MOROCCO Part I. Anostraca. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 1986, pp.125-131. ￿hal-03023908￿

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HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE MILIEU, 1986, 36 (2) : 125-131

TAXONOMICAL SIGNIFICANCE OF SCANNING ELECTRON MICROSCOPIC MORPHOLOGY OF THE EUPHYLLOPODS' RESTING EGGS FROM MOROCCO Part I. Anostraca

Graziella MURA 0> and Alain THIERY(2) (1) Department of and Human Biology, University of Rome, Italy (2) Laboratoire a"Hydrobiologie, Faculté des Sciences, B.P. S-15, Marrakech, Maroc

ANOSTRACA RÉSUMÉ. — L'étude en microscopie à balayage de la morphologie externe des œufs MAROC de durée de lOAnostracés du Maroc montre l'importance taxonomique de leur OEUFS DE DURÉE ornementation en tant que caractère d'identification au niveau spécifique. Cette MORPHOLOGIE spécificité de l'ornementation de l'enveloppe tertiaire des œufs permet alors de MICROSCOPIE À BALAYAGE confirmer la présence d'une espèce dans un biotope aquatique temporaire, même en l'absence des adultes ou lorsque l'habitat est à sec.

ANOSTRACA ABSTRACT. — Morphology of resting eggs of Anostraca from Morocco is examined MOROCCO and compared among différent species. Its taxonomical importance is stressed, indeed RESTING EGGS the eggs provide an important tool for species identification even in the absence of SCANNING ELECTRON MICROSCOPE adults or when the adult habitat is dried out. MORPHOLOGY

INTRODUCTION the number of species detected is not realistic. This led to a misunderstanding of the distribution and the ecology of the species. So far 18 species of Euphyllopoda have been reported in Morocco (Thiery and Brtek, 1985; This suggested the idea of studing the SEM Thiery, 1984, 1986 a, b); they occur at various morphology of the resting eggs of the Moroccan altitudes a.s.l. and colonise very différent kinds of species of Euphyllopoda in order to ascertain if their temporary ponds. surface pattern could be a good taxonomic tool, and consequently to fïnd a way to detect a species in a As already noted by Thiery (1986 b), in this given pond, even when the adults were absent at the country very frequently more than one species is moment of sampling, or in the absence of water. présent in the same "daya" (arab term assigned for temporary ponds of North Africa), either coexisting In the présent study the surface pattern of the or having différent life cycles. Nevertheless, depen- resting eggs of ail the Moroccan species of Anos- ding on various reasons such as the way of collecting traca has been examined by Scanning électron samples, the frequency of sampling, the relative microscopy on the whole and in détail in order to populations density and so on, on many occasions stress any possible différence. 126 G. MURA, A. THIERY

For example we compare the mean diameter of eggs coming from a brood pouch of an adult female MATERIALS AND METHODS (29.9 mm length) of Tanymastigites jbiletica and eggs recolted from desiccated mud : the différence of mean diameter between those two sorts of eggs is not The species have been determined in référence to significative (test t = 0.272, v = 58, P < 0.01). Same Daday (1910); Linder (1941); Flossner (1972) and results are available for other species : B. ferox, T. Cottarelli and Mura (1983). Three of them are new brteki, B. schaefferi... so that we could consider that species and were described by one of the authors : clean eggs taken in brood pouches of females are Thiery and Brtek (1985); Thiery (1984, 1986a). Ail alike to the dirty cysts founded in desiccated mud of ten species were confirmed by R.N. Dr. Jân Brtek of dayas. This conclusion agrées with Gilchrist (Mûzeum V. Bojniciach, Tchecoslovaquia). (1978) who noted no différence between desiccated Egg stocks used in our study were removed from and hydrated eggs in Artemia salina. the brood pouches of adult females of the following 10 species : Anémia satina (L., 1758) (Artemiidae) Branchinecta ferox (M. Edw., 1840) (Branchinectidae) Branchipus schaefferi Fisch., 1834 RESULTS Tanymasligites jbiletica Thiery & Brtek, 1985 (Branchipodidae) Tanymastigites brteki Thiery, 1985 Tanymastix affinis Daday, 1910 On the basis of our observations the resting eggs Linderiella ajricana Thiery, 1986 (Linderiellidae) Chirocephalus diaphanus Prévost, 1903 () of Moroccan fairy shrimps, according to their Streptocephalus tonicornis (Waga, 1842) var. bucheti Daday, 1910 morphological pattern, can be placed in two main (Streptocephalidae) groups : lenticular and spherical (or nearly spheri- Branchinella spinosa (M. Edw., 1840) (Thamnocephalidae) cal) shaped. This is also in good agreement with Eggs were taken directly from the ovisac of observations for Spanish (Alonso & Alcaraz, 1984) female spécimens collected from temporary ponds and Italian species (Mura et al, 1978; Mura, 1985). (natural populations). Those Anostraca were quickly As already noted for species from other countries, preserved in formaldehyde 10% to prevent pollu- spherical or nearly spherical eggs are typical of the tion, and the samples were prepared according the majority of the Anostracans, but they show very standard technique already cited in Mura et al. marked différences in diameter and shell texture (1978) and Mura (1985). from species to species (see plates I-IV). In lots of 50 cysts coming from females of Lenticular shape is typical of the eggs of Tany- différent classes of length, which is usually a good mastix affinis (Plate IA), while the remaining species determinator of âge, it appears that for each species are characterized by spherical shape. This big group the mean diameter does not vary significatively in includes globe-shaped cysts with a smooth surface any female (P < 0.05). (i.e., Artemia salina, plate IB) and a séries of va- We state also that resting eggs coming from riously ornamented surface patterns due to the dehydrated mud have the same morphology (surface présence of more or less developed ridges conver- pattern and diameter) as freshly laid eggs. ging in a number of points (Table I).

Table I. — Egg shell morphology of the Anostraca from Morocco.

Lenticular shaped . T. affinis

smooth surface A. salina ribs B. spinosa Globe shaped (big polygons) regular polygonal pattern . . T. brteki (hairs) higher ribs (more, smaller polygons) irregular polygonal pattern ornamented surface wrinkly look — B. ferox more developed ribs folded look . S. tonicornis highly developed ribs multifolded look . T. jbiletica ridges cristate look Ch. diaphanus spines spiny look L. africana very unevenly edged surface angulated look - B. schaefferi ANOSTRACA FROM MOROCCO : SEM MORPHOLOGY IN RESTING EGGS 127

Plate I. — A, above, cyst of Tanymastix affinis; below, détail enlarged. B, above, cyst of Artemia salina; below, détail enlarged.

In the case of Branchinella spinosa cysts a wrinkled appearance. Nevertheless though the (Plate IIA), the ridges are only slightly emerging, so surface ornamentation of B. spinosa and B. ferox that they look rather like "ribs", and the egg on the were very much alike, their mean diameter set them whole has a polyhedrical appearance. very clearly apart : in the first case the diameter is Tanymastigites brteki and Branchinecta ferox have 0.223 ± 0.006 mm (to 1 % threshold) while it is eggs provided with more developed ribs : in the 0.438 ± 0.006 mm (to 1 %) in the second. In Strepto- former (Plate IIB) they delineate a number of regu- cephalus torvicornis bucheti (Plate IIIA) the ridges are lar polygonal cells, while in the latter (Plate IIC) the more raised and give to the surface of the egg a polygonal cells are somewhat irregularly shaped; "folded" look; the polygonal cells they delineate are moreover, in T. brteki from the ridges originates a irregulary shaped. séries of long, thin hairs (see détail picture in The same look is typical also of the cysts of Plate IIB). Tanymastigites jbiletica (Plate III B), but in this case Compared with those of B. spinosa, the cysts of ridges are still more developed and more fréquent thèse two species look similar to some extent, but the so that the surface looks "manifold". surface pattern of the former is characterized by a The height of the ridges is very much pronounced few regular polygons, whilst T. brteki and B. ferox in Chirocephalus diaphanus (Plate IIIC), whose sur- show a great number of smaller polygons and have face pattern is quite elaborate; the polygonal cells, oo

p c > >

Plate II. — A, above, cyst of Branchinella spinosa; below, détail enlarged. B, above, cyst of Tanymastigites brteki; below, détail enlarged clearly indicating the présence of long and thin hairs on each side of the polygonal cells. C, above, cyst of Branchinecta ferox; below, détail enlarged.

130 G. MURA, A. THIERY

Plate IV. — A, above, cyst of Linderiella africana; below, détail inlarged showing the emerging "spinae". B, above, cyst of Branchipus schaefferi; below, détail enlarged.

more or less regular, delimited by the crossing of the DISCUSSION emerging ridges, have raised sides so that the egg looks somewhat "cristated". Scanning électron microscope studies of the The cysts of Linderiella africana (Plate IVA) do external morphology of the resting eggs for the not show any converging ridges but their surface is Anostracans examined in this paper provided évi- provided with a great number of conical spines dence for consistent interspecific différences and which give them a peculiar "spiny" look. confirmed the taxonomical importance of this cha- Finally, in Branchipus schaefferi (Plate IVB), the racter in identification at species level. eggs have a completely différent appearance, since Our data for Morocco are mainly in good agree- their surface is very unevenly edged; there are ment with Alonso & Alcaraz's observations for fairy neither ribs nor ridges, but dépressions and reliefs shrimps from Iberia peninsula (except for the diame- alternating giving it an "angulated look". The same ter of Branchinecta ferox's eggs which is half of results have been shown by Gilchrist (1978). In this Moroccan eggs) (Alonso and Alcaraz, 1984). They study, the diameter of eggs (âge or length of cultured also agrée with the results found on English species females unknowed) is 0.25 mm, therefore in Moroc- (Branchipus stagnalis L. (= B. schaefferi Fisch., and can populations the mean diameter is Artemia salina) by Gilchrist (1978) and on American 0.253 mm ± 0.007 (to 1 % threshold). stump of Artemia salina by Mazzini (1978). At last ANOSTRACA FROM MOROCCO : SEM MORPHOLOGY IN RESTING EGGS 131 they agrée with data available for Italian species Tierwelt Deutschlands, Veb Gustav Fischer Verlag Jena (Mura et al, 1978; Mura, 1985). We can therefore Ed., 60 : 1-501. infer that as far as Moroccan species are concerned, GILCHRIST B., 1978. Scanning électron microscope studies it is possible to detect the présence of a given species of the egg shell in some Anostraca (Crustacea, Bran- even in the absence of adult spécimens or of water chiopoda). Cell. Tiss. Res., 193 : 337-351. in the ponds. It would be now interesting to investi- LINDER F. 1941. Contributions to the morphology and the gate also, the species of other Euphyllopods (Notos- of the Anostraca. Zool Bidr. traca and Conchostraca) occurring in Morocco to Uppsala, 20 : 101-302. know if it is possible to extend to their eggs the MAZZINI M. 1978. — Scanning électron microscope validity of the above considered character. morphology and amino-acid analysis of the egg-shell of encysted Brine shrimp Artemia salina Leach (Crusta- cea, Anostraca). Monitore Zool. Ital. (N.S.), 12 : ACKNOWLEDGEMENTS. The authors are indebted to 243-252. the Centro di Studio per la Geologia dell'Italia MURA G., F. ACCORDI & M. RAMPINI, 1978. Studies on the Centrale (C.N.R.) for the use of the scanning élec- resting eggs of some freshwater fairy shrimps of the tron microscope, and particularly to Alfredo Man- genus Chirocephalus : biometry and scanning électron cini for his kind help in the préparation and microscopic morphology (Branchiopoda, Anostraca). observation of the spécimens. Crustaceana, 35 (2) : 190-194.

MURA, 1985. SEM morphological survey on the egg shell in the Italian species of Anostracans. Hydrobiologia (in press). REFERENCES THIERY A. & J. BRTEK, 1985. Tanymastigites jbiletica n.sp. from Morocco. (Anostraca, Branchipodidae). Annot. zool. bot. Bratislava, 164 : 1-4. ALONSO M. & M. ALCARAZ, 1984. Huevos resistentes de THIERY A. Un nouveau Branchiopode Anostracé des eaux Crustaceos Eufilopodos no Cladoceros de la peninsula stagnantes temporaires du Maroc : Tanymastigites Iberica : observacion de la morfologia externa me- brteki n.sp. Frag. Entomol. (in press). diante tecnicas de microscopia electronica de barrido. THIERY A., 1986 a. Linderiella africana n.sp., premier Oecologia aquatica, 7 : 73-78. représentant des Linderiellidae (Crustacea, Anostraca) COTTARELLI V. & G. MURA, 1983. Anostraci, Notostraci, en Afrique du Nord (Maroc) Crustaceana, 51 (1) in Concostraci (Crustacea : Anostraca, Notostraca, press. Conchostra) in Guide per il riconscimento délie specie THIERY A., 1986b. Les Crustacés Branchiopodes Ano- animali délie acque interne Italiane. Consiglio Nazio- straca, Notostraca et Conchostraca du Maroc occi- nale délie Ricerche AQ/1/194. 18 : 1-73. dental : I inventaire et répartition. Bull. Soc. Hist. Nat. DADAY DE DEES E., 1910. Monographie systématique des Toulouse, 122, (in press). Phyllopodes Anostracés. Ann. Se. Nat. Zool., Série 9, 9 : 91-489. FLOSSNER D., 1972. Krebstiere, Crustacea, Kiemen-und Reçu le 4 mars 1985; received Mardi 4, 1985 Blattfusser, Branchiopoda Fischlause, Branchiura. Accepté le 20 novembre 1985; accepted November 11, 1985