Rotifera X Developments in Hydrobiology 181

Series editor K. Martens Rotifera X Research: Trends, New Tools and Recent Advances

Proceedings of the Xth International Rotifer Symposium, held in Illmitz, Austria, 7–13 June 2003

Edited by Alois Herzig,1 Ramesh D. Gulati,2 Christian D. Jersabek3 & Linda May4

1Biological Station Neusiedler See, Illmitz, Austria 2NIOO, Centre of Limnology, Nieuwersluis, The Netherlands 3University of Salzburg, Austria 4Centre for Ecology and Hydrology, Penicuik, Midlothian, Scotland

Reprinted from Hydrobiologia, volume 546 (2005)

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A C.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN 1-4020-3493-8

Published by Springer, P.O. Box 17, 3300 AA Dordrecht, The Netherlands

Cover illustration: Hexarthra polyodonta, drawing by Walter Koste

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Printed in the Netherlands TABLE OF CONTENTS

Preface xi–xiv Photo of participants xiv Walter Koste – a K-strategist? A laudatio N. Walz 1–8

PART I: PHYLOGENY AND EVOLUTION On the phylogenetic position of Rotifera – have we come any further? P. Funch, M.V. Sørensen, M. Obst 11–28 Speciation and selection without sex C.W. Birky Jr., C. Wolf, H. Maughan, L. Herbertson, E. Henry 29–45 Bayesian and maximum likelihood analyses of rotifer–acanthocephalan relationships D.B. Mark Welch 47–54 Evolutionary dynamics of ‘the’ bdelloid and monogonont rotifer life-history patterns C.E. King, C. Ricci, J. Schonfeld, M. Serra 55–70 Toward a better understanding of the phylogeny of the Asplanchnidae (Rotifera) E.J. Walsh, R.L. Wallace, R.J. Shiel 71–80

PART II: GENETICS AND MOLECULAR ECOLOGY Molecular ecology of : from population differentiation to speciation A. Go´mez 83–99 The potential of genomic approaches to rotifer ecology D.B. Mark Welch, J.L. Mark Welch 101–108 Using amplified fragment length polymorphisms (AFLP) to study genetic variability in several freshwater rotifer species S. Herna´ndez-Delgado, N. Mayek-Pe´rez, G.E. Santos-Medrano, R. Rico-Martı´nez 109–115 Molecular characterization of Mn-superoxide dismutase and gene expression studies in dietary restricted Brachionus plicatilis rotifers G. Kaneko, T. Yoshinaga, Y. Yanagawa, S. Kinoshita, K. Tsukamoto, S. Watabe 117–123 Behavioural reproductive isolation in a rotifer hybrid zone H.K. Berrieman, D.H. Lunt, A. Go´mez 125–134

PART III: TAXONOMY AND BIOGEOGRAPHY The ‘Frank J. Myers Rotifera collection’ at the Academy of Natural Sciences of Philadelphia C.D. Jersabek 137–140 vivi

Tale of a sleeping beauty: a new and easily cultured model organism for experimental studies on bdelloid rotifers H. Segers, R.J. Shiel 141–145 Life on the edge: rotifers from springs and ephemeral waters in the Chihuahuan Desert, Big Bend National Park (Texas, USA) R.L. Wallace, E.J. Walsh, M.L. Arroyo, P.L. Starkweather 147–157

PART IV: MORPHOLOGY AND ULTRASTRUCTURE Euryhaline Brachionus strains (Rotifera) from tropical habitats: morphology and allozyme patterns T. Kotani, A. Hagiwara, T.W. Snell, M. Serra 161–167 Morphological and morphometrical variations of selected rotifer species in response to predation: a seasonal study of selected brachionid species from Lake Xochimilco (Mexico) G. Garza-Mourin˜o, M. Silva-Briano, S. Nandini, S.S.S. Sarma, M.E. Castellanos-Pa´ez 169–179 Morphological stasis of two species belonging to the L-morphotype in the Brachionus plicatilis species complex S. Campillo, E.M. Garcı´a-Roger, D. Martı´nez-Torres, M. Serra 181–187 Morphological variation of Keratella cochlearis (Gosse) in a backwater of the River Thames J. Green 189–196 Trophi structure in bdelloid rotifers G. Melone, D. Fontaneto 197–202 Study of the trophi of Testudinella Bory de St. Vincent and Pompholyx Gosse (Rotifera: Testudinellidae) by scanning electron microscopy W.H. De Smet 203–211 Do rotifer jaws grow after hatching? D. Fontaneto, G. Melone 213–221 External morphology and muscle arrangement of Brachionus urceolaris, , Hexarthra mira and Notommata glyphura (Rotifera, ) N. Santo, D. Fontaneto, U. Fascio, G. Melone, M. Caprioli 223–229 The musculature of Testudinella patina (Rotifera: Flosculariacea), revealed with CLSM M.V. Sørensen 231–238 Rotifer nervous system visualized by FMRFamide and 5-HT immunocytochemistry and confocal laser scanning microscopy E.A. Kotikova, O.I. Raikova, M. Reuter, M.K.S. Gustafsson 239–248 Identification of acetylcholinesterase receptors in Rotifera A. Pineda-Rosas, G.E. Santos-Medrano, M.F. Zavala-Reynoso, R. Rico-Martı´nez 249–253 vii

PART V: MATING, RESTING EGGS, DIAPAUSE, ANHYDROBIOSIS, EMBRYONIC DEVELOPMENT Brachionus calyciflorus is a species complex: Mating behavior and genetic differentiation among four geographically isolated strains J.J. Gilbert, E.J. Walsh 257–265 Removal of surface glycoproteins and transfer among Brachionus species T.W. Snell, C.-P. Stelzer 267–274 Maternal effect by stem females in Brachionus plicatilis: effect of starvation on mixis induction in offspring A. Hagiwara, Y. Kadota, A. Hino 275–279 Restoration of tropical peat swamp rotifer communities after perturbation: an experimental study of recovery of rotifers from the resting egg bank S. Chittapun, P. Pholpunthin, H. Segers 281–289 Diapause in monogonont rotifers T. Schro¨der 291–306 Anhydrobiosis of Adineta ricciae: costs and benefits C. Ricci, C. Covino 307–314 A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers A. Tunnacliffe, J. Lapinski, B. McGee 315–321 The development of a bdelloid egg: a contribution after 100 years C. Boschetti, C. Ricci, C. Sotgia, U. Fascio 323–331

PART VI: POPULATION AND COMMUNITY ECOLOGY Evolution of rotifer life histories C.-P. Stelzer 335–346 Insulin-like growth factor signaling pathway involved in regulating longevity of rotifers T. Yoshinaga, G. Kaneko, S. Kinoshita, S. Furukawa, K. Tsukamoto, S. Watabe 347–352 Combined effects of algal (Chlorella vulgaris) food level and temperature on the demography of Brachionus havanaensis (Rotifera): a life table study E.L. Pavo´n-Meza, S.S.S. Sarma, S. Nandini 353–360 Factors affecting egg-ratio in planktonic rotifers S.S.S. Sarma, R.D. Gulati, S. Nandini 361–373 Factors affecting swimming speed in the rotifer Brachionus plicatilis M. Yu´fera, E. Pascual, J.M. Olivares 375–380 An evidence for vertical migrations of small rotifers – a case of rotifer community in a dystrophic lake A. Karabin, J. Ejsmont-Karabin 381–386 Structure distinctions of pelagic rotifer plankton in stratified lakes with different human impact G.A. Galkovskaya, I.F. Mityanina 387–395 viii

Changes in rotifer species composition and abundance along a trophic gradient in Loch Lomond, Scotland, UK L. May, M. O’Hare 397–404 Diversity and abundance of the planktonic rotifers in different environments of the Upper Parana´ River floodplain (Parana´ State – Mato Grosso do Sul State, Brazil) C.C. Bonecker, C.L. Da Costa, L.F.M. Velho, F.A. Lansac-Toˆha 405–414 Relationships between rotifers, phytoplankton and bacterioplankton in the Corumba´ reservoir, Goia´s State, Brazil C.C. Bonecker, A.S.M. Aoyagui 415–421 Short time-response of psammic communities of Rotifera to abiotic changes in their habitat J. Ejsmont-Karabin 423–430 The influence of biotic and abiotic factors on psammic rotifers in artificial and natural lakes I. Bielan´ska-Grajner 431–440

PART VII: LONG-TERM STUDIES Seasonal rotifer dynamics in the long-term (1969–2002) record from Lake Kinneret (Israel) M. Gophen 443–450 Seasonality of rotifers and temperature in Lough Neagh, N. Ireland T.E. Andrew, J.A.M. Andrew 451–455 Abiotic vs. biotic factors: lessons drawn from rotifers in the Middle Loire, a meandering river monitored from 1995 to 2002, during low flow periods N. Lair 457–472

PART VIII: TROPHIC INTERACTIONS Freshwater copepods and rotifers: predators and their prey Z. Brandl 475–489 Life history characteristics of Asplanchnopus multiceps (Rotifera) fed rotifer and cladoceran prey S. Nandini, S.S.S. Sarma 491–501 Susceptibility of ephemeral pool Hexarthra to predation by the fairy shrimp Branchinecta mackini : can predation drive local extinction? P.L. Starkweather 503–508 Decline of clear-water rotifer populations in a reservoir: the role of resource limitation M. Devetter, J. Sed¢a 509–518 Combined effects of food concentration and temperature on competition among four species of Brachionus (Rotifera) M.A. Ferna´ndez-Araiza, S.S.S. Sarma, S. Nandini 519–534 Application of stable isotope tracers to studies of zooplankton feeding, using the rotifer Brachionus calyciflorus as an example A.M. Verschoor, H. Boonstra, T. Meijer 535–549 ix

PART IX: AQUACULTURE AND ECOTOXICOLOGY Screening methods for improving rotifer culture quality A. Araujo, A. Hagiwara 553–558 Interaction among copper toxicity, temperature and salinity on the population dynamics of Brachionus rotundiformis (Rotifera) J.L. Gama-Flores, S.S.S. Sarma, S. Nandini 559–568 Effect of some pesticides on reproduction of rotifer Brachionus plicatilis Mu¨ ller H.S. Marcial, A. Hagiwara, T.W. Snell 569–575 Heat shock protein 60 (HSP60) response of Plationus patulus (Rotifera: Monogononta) to combined exposures of arsenic and heavy metals J.V. Rios-Arana, J.L. Gardea-Torresdey, R. Webb, E.J. Walsh 577–585 Subject Index 587–595 Rotifer Species Index 597–601 Hydrobiologia (2005) 546:xi–xiv Springer 2005 A. Herzig, R.D. Gulati, C.D. Jersabek & L. May (eds.) Rotifera X: Rotifer Research: Trends, New Tools and Recent Advances DOI 10.1007/s10750-005-4085-6

Preface

The Xth International Rotifer Symposium was occasion was made all the more enjoyable by the held in Illmitz, Austria, 7–13 June 2003, at the wonderful atmosphere created by a brass band Information Centre of the National Park Neusied- playing music typical of Czech Republic, Slovakia ler See – Seewinkel. The Symposium was returning and eastern Austria. A full-day excursion was to Austria 27 years after the first rotifer meeting organized on the Wednesday. The participants was organized there by Prof. Agnes Ruttner- enjoyed a cruise around Neusiedler See, a visit Kolisko at the Biological Station Lunz in 1976. and an introduction to the activities of the Wine The Xth meeting was attended by 113 participants Academy at Rust (which runs courses in the from 28 countries. It was organized by Alois Science of Wine Making) combined with a short Herzig with the assistance of Christian Jersabek, wine tasting, a guided tour through the old town Institute of Zoology, University of Salzburg and of Rust (buildings dating back to the 16th cen- Alois Lang, Information Centre of the National- tury), and a visit to the Baroque Esterha´ zy Palace park Neusiedler See – Seewinkel. It was hosted by at Eisenstadt. As an preamble to Joseph Haydns the Biological Station Neusiedler See (Provincial music, a chamber concert was given in the fa- Administration of Burgenland) and the National mous Haydn Hall of the Esterha´ zy Palace. Par- Park Society. The symposium venue provided an ticipants were invited to a lunch by the Head of excellent opportunity for the community of rotifer the Government of the Province of Burgenland, researchers to follow the scientific programme which took place in representative rooms of the combined with enjoyable breaks and nice sund- Palace. The excursion in the afternoon to Hun- owners. gary included a visit to typical farm houses in a After the opening ceremony and a short small village situated south of Neusiedler See appraisal by Alois Herzig of the contents and (Ferto¨ sze´ plak) and the baroque Esterha´ zy Castle topics of the last nine meetings, Norbert Walz paid of Ferto¨ d, the place where Haydn spent nearly a tribute to the life-time works of Walter Koste. two decades of his creative life. The Conference Subsequently, the scientific programme followed Dinner was hosted by the Government of the traditions of the previous symposia with 6 the Province of Burgenland on Friday at invited main lectures, 56 oral contributions and 45 Johanneszeche, a typical restaurant with Hun- poster presentations. The papers were grouped garian ambience and Croatian (Tamburizza) and into thematic sessions: Phylogeny, evolution and gipsy music in the backdrop. Accompanying genetics; Molecular ecology; Biogeography and guests made several day trips to places of natural, development; Diapause, anhydrobiosis and resting cultural and historical interests in the Neusiedler eggs; Morphology, ultrastructure and behaviour; See area and the adjacent Hungarian neighbour- Feeding; Population ecology; Culture of rotifers; hood townships. Physiology and ecotoxicology. In addition, two Kluwer Academic Publishers, now Springer late afternoon sessions were devoted to the careers Aquatic Sciences, and Prof. Dr. Koen Martens, in rotiferology of John Gilbert and Henri Dumont. Editor-in-chief Hydrobiologia, have accepted to Special thanks to John J. Gilbert, Ramesh D. publish the symposium proceedings as a special Gulati, Charles E. King, Linda May, Claudia volume in the series Developments in Hydrobiology. Ricci, Terry W. Snell and Robert L. Wallace for The manuscripts accepted for publication have their involvement with the arrangements for the undergone a careful review and revision process scientific programme. and appropriate editorial amendments needed for Social activities began with a Welcome clarity and conciseness. The final product is the Party that was held on Saturday evening at the result of the efforts of the authors, reviewers, edi- Information Centre of the National Park. The tors and the Editor-in-chief. xii

The Proceedings are composed of nine parts J.L. Mark Welch discuss in their paper the appli- (See Contents). The introductory paper by Funch cation of two genomic-based tools used in surveys et al. (Part I) offers a detailed discussion of the of microbial communities to rotifer taxonomy: phylogenetic position of rotifers vis-a-vis gnathi- serial analysis of gene tags (SAGT) and micro- feran groups. Originally, Gnathifera only com- array hybridization. They also report the con- prised the hermaphroditic Gnathostomulida and struction and hybridization of a small microarray the Syndermata. On the basis of the ultrastructure of rotifer sequences, thereby demonstrating that of the trophy, the rotifers belong to the Gnathi- these techniques are most powerful if combined fera; moreover, molecular evidence strongly sug- with traditional rotifer systematics. gests that they are closely related to the parasitic Bdelloids show a rather uniform morphology acanthocephalans and the two together form the of jaws (trophi), most recognizably feature is the clade Syndermata. In his paper Mark Welch pro- presence of a series of teeth forming unci plates, vides evidence for a monophyletic Eurotatoria each with one to ten major median teeth. Using based on maximum likelihood and Bayesian SEM photomicrographs of trophi and literature analysis of the protein-coding gene hsp82 and for data, Melone and Fontaneto deduce that few the placement of within the Phy- major teeth are common in species living in water lum Rotifera as a sister clade to either Eurotatoria bodies, where these species possibly eat unicellular or Seisonidea. algae, while more major teeth are more common in Substantial differences in both life-table char- species inhabiting mosses and lichens, where they acteristics and reproductive patterns distinguish possibly consume bacteria. bdelloid rotifers from monogonont rotifers. Modern techniques can contribute significantly King et al. explore some of the adaptive conse- to our understanding of the rotifers anatomy, quences of these life-history differences using a especially relating to the musculature and the computer model to simulate the evolutionary nervous system. Very recently, immunostaining acquisition of new beneficial mutations. Birky has been applied in combination with confocal et al., isolated more than 100 females of the obli- laser scanning microscopy (CLSM). Santo et al., gately asexual bdelloid rotifers from nature and applied CLSM to describe the muscle arrangement sequenced their mitochondrial cox1 genes and of Brachionus urceolaris, Floscularia ringens, conclude that in the absence of sexual reproduction Hexarthra mira and Notommata glyphura. Søren- the bdelloids have undergone substantial clado- sen describes the musculature of Testudinella genesis; bdelloid clades are adapted to different ni- patina. Kotikova et al. presents data on the ches and have undergone substantial speciation. immuno-reactivity patterns in the nervous system The authors failed to detect a decrease in the effec- of Platyas patulus, Euchlanis dilatata and tiveness of natural selection on bdelloid genes. Asplanchna herricki using CLSM. That species The development of cost-effective molecular considered to be cosmopolitan can be complexes tools that allow the amplification of minute of sibling species has been recently clearly dem- amounts of DNA, effectively opened the field of onstrated for the rotifer Brachionus plicatilis: molecular ecology of rotifers. In Part II (Genetics within the Iberian Peninsula three species have and Molecular Ecology), Go´ mez critically reviews: been described and another three have been iden- (1) methodological advances that have facilitated tified (see Go´ mez, Part II). Gilbert and Walsh who the application of molecular techniques to rotifers, observed mating behaviour and genetic differenti- (2) recent advances in the field of rotifer molecular ation among four geographically isolated strains ecology, and (3) future developments and areas of Brachionus calyciflorus conclude that it is a which are likely to benefit further from the species complex in which some geographically and molecular ecological approach. It is now feasible genetically distinct strains are reproductively iso- to obtain representative DNA sequences from lated from one another. identified rotifer species for use in genomic-based Bdelloid rotifers can withstand desiccation by surveys for determining rotifers in new sample entering a state of suspended animation: anhy- collections, circumventing the difficulties that go drobiosis. Ricci and Covino describe and discuss with traditional surveys. D.B. Mark Welch and costs and benefits of anhydrobiosis of a new xiii species, Adineta ricciae, a new species described by previous Rotifer Symposia as well as contributed a Segers and Shiel (see part III). A comparison of paper to this volume. On behalf of the rotifer this with Macrotrachela quadricornifera reveals family, we extend our profound sympathy to both species suspend their life activities during Andrzej’s wife, Jolanta Ejsmont-Karabin. desiccation as well do not ‘‘age’’ during anhydro- The editors wish to thank the ‘‘local organiz- biosis. This meets the prediction of the ‘‘Sleeping ers’’ for their invaluable help during the sympo- Beauty’’ model. Anhydrobiosis is thought to sium. They also wish to acknowledge the require accumulation of the non-reducing disac- Government of the Province of Burgenland for charides trehalose (in and fungi) or financial support. sucrose (in plant seeds and resurrection plants), which may protect proteins and membranes by The Editors acting as water replacement molecules and vitri- fying agents. However, in clone cultures of the Alois Herzig bdelloids Philodina roseola and Adineta vaga Ramesh D. Gulati Tunnacliffe et al. were unable to detect trehalose Christian D. Jersabek or other disaccharides. Instead, on dehydration, Linda May P. roseola upregulates a hydrophilic protein related to the late embryogenesis abundant (LEA) proteins associated with desiccation tolerance in List of Reviewers plants. It could well be that hydrophilic biosyn- thesis represents a common element of anhydro- Ahlrichs, W. biosis. Andrew, T.E. A number of studies examine spatial and tem- Birky, Jr., C.W. poral variability in rotifer abundance and com- Carmona, M.J. munity structure in relation to variations in abiotic Carvalho, G.R. and biotic factors along gradients in natural water De Meester, L. bodies, and in laboratory. M. Gophen presents the De Paggi, J. results of a long-term study on seasonal rotifer De Smet, W.H. dynamics in Lake Kinneret (Israel) and T.E. Dingmann, B.J. Andrew and J.A.M. Andrew in Lough Neagh Duggan, I.C. (Northern Ireland). N. Lair focussed on rotifers in Dumont, H.J. river plankton, especially the response of various Ejsmont-Karabin, J. rotifer taxa to hydraulic conditions, and the role of Ferrando, M.D. rotifers in the river food web. Fussmann, G. As a special topic, Z. Brandl reviews the Gilbert, J.J. trophic relationship between freshwater copepods Go´ mez, A´ . and rotifers. Most copepod species, at least in Gophen, M. their later developmental stages, predate Green, J. efficiently, preferably on rotifers. Generally, soft- Gulati, R.D. bodied species of rotifers are more vulnerable Hagiwara, A. to predation than those that possess spines or Hampton, S.E. lorica. But also behavioural characteristics, e.g., Herzig, A. movements and escape reactions, and temporal Hessen, D. and spatial distribution of rotifers are important in Jersabek, C.D. these trophic interactions. The reported predation Joaquim-Justo, C. rates by freshwater copepods can effectively exer- King, C.E. cise a top-down control of rotifer populations. Lair, N. During the preparation of the present pro- Lubzens, E. ceedings, we heard about the sudden death of Mark Welch, D.B. Andrzej Karabin, who had designed logos for May, L. xiv

Melone, G. Segers, H. Miracle, M.R. Serra, M. Morales-Baquero, R. Shiel, R.J. Nandini, S. Snell, T.W. Nogrady, T. Starkweather, P.L. Ortells, R. Stemberger, R. Raikova, O.I. Tunnacliffe, A. Rao, T.R. Van der Stap, I. Reckendorfer, W. Viroux, L. Ricci, C. Wallace, R.L. Rico-Martinez, R. Walsh, E.J. Rieger, R. Walz, N. Sanoamuang, L. Wilke, T. Sarma, S.S.S. Winkler, H. Schmid-Araya, J.M. Yu´ fera, M. Schro¨ der, T. Zimmermann-Timm, H.