Bulletin of the SCANDINAVIAN SOCIETY

FOR PARASITOLOGY

WITH PROCEEDINGS FROM SSP SPECIAL SYMPOSIUM, PARASITES AND ECOLOGY OF MARINE AND COASTAL , STYKKISHOLMUR, ICELAND 15-18 JUNE 1996 Vol. 6 No. 2 1996 for of

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r - EMO , AAAM ATUKOGI · PROCEEDINGS

of the symposium on

PARASITES AND ECOLOGY OF MARINE AND COASTAL BIRDS,

arranged on behalf of the

Scandinavian Society for Parasitology

in Stykkish6lmur, Iceland

June 15 -June 18, 1996

Editors: Karl Skfrnisson and Arne Skorping

Organizing and Scientific Secretariat: Institute for Experimental Pathology, Keldur, University of Iceland, IS-112 Reykjavik, Iceland. Tel: +354 567 4700, Fax: +354 567 3979, e-mail: [email protected] ii

Scientific Programme and Organizing Committee:

Karl Skirnisson, Keldur, University of Iceland, Reykjavik, kcland

(chairman)

Kurt Buchmann, RVA University of Copenhagen, Denmark

Hans-Peter Fagerholm, Abo Academy University, Finland

Arne Skorping, University of Tromsl<), Norway

Jan Thulin, Inst. of Marine Research, Lysekil, Sweden

Local Organizing Committee:

Karl Skirnisson, Keldur, University of Iceland, Reykjavik, Iceland

(Chairman)

Arn6r I>6rir Sigfusson, Icelandic Institute of Natural History,

Reykjavik, Iceland

Kristinn H. Skarpheoinsson, Icelandic Institute of Natural History,

Reykjavik, Iceland

Sponsors:

The generous support from the following sponsors is gratefully acknowledged:

-The Scandinavian Society for Parasitology (SSP)

-Nordic Academy for Advanced Studies (NorFA)

-Nordic Council fo r Wildlife Research (NKV)

-Clara Lachmanns Fond, Sweden

-The Icelandic Ministry of Agriculture

-The Icelandic -breeder's Association

- The Town of Stykkisholmur

-Inst. for Experimental Pathology, Keldur, University of

Iceland iii IV

PREFACE

During June 15-18, 1996 a special symposium on Parasites 111111 Fm/ogy r�f

Marine and Coastal Birds was held on behalf of the Scandinavian SociL· Ly for Parasitology in Stykkish6lmur, Iceland. This was the second spGcial syn1posium arranged in Iceland on behalf of the Society. The first one dealt with Parasitl's of biological and economic significance in the aquatic environment, - Thirty years (�l research and fu ture trends- and was held on Heimaey in the Westmann Islands July 2

- 6, 1994. The purpose of the symposium on Parasites and Ecology of Marine and Coastal Birds was to bring together parasitologists, ecologists and ornithologist for the exchange of ideas and information and to develop cooperative projects in marine and coastal ecology. Papers based on the plenary lectures given by the invited speakers as well as the abstracts of the submitted oral and poster presentations are published in this special ISSUe. Participants are thanked for their valuable contributions to the success of the symposium. Furthermore the organizing committees wish to thank the Iceland Tourist Bureau (ITB Congrex) in Reykjavik and all the helpful individuals involved in the practical planning and accomplishment of the symposium for valuable assistance. Last but not least we wish to express our deepest gratitude to the sponsors of the symposium. Their financial aid made the symposium possible and supported the participation of many scientists which considerably increased the scientific value of the meeting. Support from the Scandinavian Society for Parasitology, NorFA, NKV and the Clara Lachmanns Fond made it possible to produce an unusually thick and informative issue of the SSP Bulletin.

Autumn 1996 K. Skfrnisson A. Skorping V

CONTENTS

INVITED LECTURES Factors influencing the prey choice of marine birds in multiple prey situations

Bustnes, }an Ove ...... I parasites of marine- and shore birds, and their role as pathogens

Fagerholm, Hans-Peter ...... 16 Life cycles and distribution of seabird helminths in arctic and sub-arctic regions

Galaktionov, Kirill V ...... 31 Impact of seabird helminths on host populations and coastal ecosystems

Galaktionov, Kirill V ...... , .... 50 Fauna! diversity among avian parasite assemblages: The interaction of history, ecology, and biogeography in marine systems

Hoberg, Eric P...... 65 The common eider: Ecological and economical aspects

Skarpheoinsson, Kristinn Haukur ...... 90 Why should marine and coastal bird ecologists bother about parasites?

Skorping, Arne ...... 98 Ecological implications of Hematozoa in birds

Valkiiinas, Gediminas ...... 103

SUBMITTED PAPER Trematode infestation as a factor in shorebird oversummering: A case study of the greater yellowlegs (Tringa melanoleuca) McNeil, Raymond, Marcos T. Dfaz, Belkys Casanova, Michel Thibault &

A lain Villeneuve ...... 114

SUBMITTED ABSTRACTS OF ORAL AND POSTER PRESENTATIONS The Acuarioid (Acuarioidea) of the upper digestive tract of New World waders and their transmission in marine environments

Anderson, R.C. & P.L. Wong ...... 118 Ephemerality in Filarioid nematodes (Eulimdana spp.) found subcutaneously in charadriiforms and transmitted by lice

Bartlett, CherylM ...... 118 A new trematode of the family Philophthalmidae Travassos, 1918 in the American oystercatcher, Haematopus palliatus in the North-East coastal of Venezuela

Dfaz, Marcos Tulio & Ramos, Susana ...... 119 vi

Ticks Ixodes uriae and their participation in circulation of arbovimses in hrcL�ding colonies on the Barents Sea coast

Efremova, Galina & Alexander Gembitzky* ...... /20 Gulls (Laridae) in Iceland as final hosts for digenean trematodes

Eydal, Matthlas, Brynja Gunnlaugsd6ttir & Droplaug Olafsd6ttir ...... 120 The role of Black Sea marine and coastal birds in infections of fish and molluscs with trematodes Gaevskaja, Albina & Vladimir Machkevsky* ...... 121 Gut parasite load and diet of waders: Methods and first results Le Drean-Quenec'hdu, Sophie & John Goss-Custard ...... 122 The role of different gammarid communities in transmission of minutus () to

Lehtonen, Jukka T...... 122 Monitoring of seabirds hibernating in Sevastopol's bays Machkevsky, Vladimir & Roman Machkevsky* ...... 123 Experimental infestation of sea-gulls by eye-flukes from the three-spined stickleback Morozinska-Gogol, Jolanta & Jerzy Rokicki ...... 123 Nematode infections in Icelandic seabirds Olafsd6ttir, Droplaug, Kristjdn Lilliendahl & J6n S6lmundsson ...... 124 Pathological studies on common eiders from Skerjafjorour, Iceland. Siguroarson, Sigurour, Slavko Helgi Bambir, Karl Sklrnisson & Arn6r P6rir Sigfusson ...... 125 Parasites and ecology of the common eider in Iceland. Skfrnisson, Karl & Aki A. J6nsson ...... 126 Seasonal changes of the food composition and condition of the common eider in Iceland Skfrnisson, Karl , Aki A. J6nsson, Arn6r P. Sig[Usson & Sigurour Siguroarson ...... 127 Mortality associated with renal and enteric coccidiosis in juvenile common eiders in Iceland

Skfrnisson, Karl, Sigurour Siguroarson, Slavko H. Bambir & Arn6r P. Sigfusson... 128 The rhinonyssid mites (Gamasina: Rhinonyssidae) of some marine and coastal birds Maria Stanyukovich ...... 129

CONCLUDING REMARKS

Buchmann, Kurt ...... 130

* Authors cancelled participation but asked for printing of submitted abstracts. vii

LIST OF PARTICIPANTS Anderson, Roy C. University of Guelph, Department of Zoology, Guelph, Ontario, Canada NIG 2Wl Bambir, Slavko Helgi Institute for Experimental Pathology, Keldur, University of Iceland, IS-112 Reykjavik, Iceland Bartlett, Cheryl M. Biology, University College of Cape Breton, Biology UCCB, Box 5300, Sydney, Nova Scotia, Canada BIP 6L2 Buchmann, Kurt The Royal Veterinary and Agricultural University, Department of Veterinary Microbiology, Btilowsvej 13, DK- 1870 Frederiksberg C, Denmark Bustnes, Jan Ove Foundation for Nature Research and Cultural Heritage Research, Department of Arctic Ecology, Storgt. 25, N-9005 Troms0, Norway Dfaz, Marcos Tulio Instituto de Investigaciones Biomedicas y Ciencias Aplicadas, Universidad de Oriente, Cumana, Estado Sucre, Venezuela Eydal, Matthfas Institute for Experimental Pathology, Keldur, University of Iceland, IS-112 Reykjavik, Iceland Fagerholm, Hans-Peter Institute of Parasitology, Dept. Bioi., Abo Akademi University, Artillergatan 6, BioCity, 20520 Abo, Finland Galaktionov, Kirill V. Murmansk Marine Biological Institute, Russian Academy of Science, 17 Vladimirskaya St., Murmansk, Russia Hauksson, Erlingur Marine Research Institute, Skulagata 4, IS-I 01 Reykjavik, Iceland Hoberg, Eric P. Biosystematics and National Parasite Collection Unit, Livestock & Poultry Sciences Institute, Agricultural Research Service, United States Department of Agriculture, Rm. 102, Bldg. 1180, BARC-East, Beltsville, MD 20705-2350, Maryland, USA J 6nsson, Aki A. Wildlife Management Institute, Hafnarstrceti 97, IS-600 Akureyri, Iceland. Le Drean-Quenec'hdu, Sophie Laboratoire d'Evolution des Systemes Naturels et Modifies, Universite de Rennes I, A venue du General Leclerc, 35042 Rennes cedex, France ' viii

Lehtonen, Jukka T. Department of Ecology and Systematics, Division of Population Biology, P.O. Box 17, FIN-00014 University of Helsinki, Finland McNeil, Raymond Department of Biological Sciences, University of Montreal, C.P. 6128, Succ. "Centre­ ville", Montreal, Quebec, Canada H3C 317 6lafsd6ttir, Droplaug Marine Research Institute, Skulagata 4, IS-I 01 Reykjavik, Iceland Richter, Sigurour H. Institute for Experimental Pathology, Keldur, University of Iceland, IS-1 12 Reykjavik, Iceland Rokicki, Jerzy Department of Invertebrate Zoology, University of Gdansk, Al. Marszalka Pilsudskiego 46, 81-378 Gdynia, Poland

Sigfiisson, Arn6r .P. Icelandic Institute of Natural History, Hlemmur 3, IS-101 Reykjavik, Iceland Siguroarson, Sigurour Central Veterinary Laboratory, Keldur, IS-112 Reykjavik, Iceland Skarpheoinsson, Kristinn Haukur Icelandic Institute of Natural History, Hlemmur 3, IS-101 Reykjavik, Iceland Skfrnisson, Karl Institute for Experimental Pathology, Keldur, University of Iceland, IS-1 12 Reykjavik, Iceland Skorping, Arne Department of Ecology/Zoology, IBG, University of Tromsp, N-9037 Norway Snrebji:irnsson, Arni The Icelandic Eider breeder's Association, Brendasamti:ikI slands, Brendahi:illinnivio Hagatorg, IS-107 Reykjavik, Iceland Stanyukovich, Maria Zoological Institute of Russian Academy of Sciences, St Petersburg, University Enbankment 1, St Petersburg 199034, Russia Valkiunas, Gediminas Institute of Ecology, Lithuanian Academy of Sciences, Akademijos 2, Vilnius 2600, Lithuania Bull Scand Soc Parasitol1996; 6 (2): 1-15

FACTORS INFLUENCING THE PREY CHOICE OF MARINE BIRDS IN MULTIPLE PREY SITUATIONS

Jan Ove Bustnes Foundation for Nature Research and Cultural Heritage Research, Department of Arctic Ecology, Storgt. 25, N-9005 Troms0, Norway

Abstract Different of marine birds with quantitative predictions, and they exploit different feeding and will show how the availability of diffe­ prey types in the marine environment. rent prey items, prey quality, time Most alcids and petrels feed on fish in constraints, danger of predation, internal the open sea, while the cormorants, the state of the , kleptoparasitism and terns, some gulls, and sea ducks feed on risk of ingesting parasites may influence fish and invertebrates in inshore waters. the prey choice of marine birds. The The shorebirds and many gulls feed on conclusion is that all these factors invertebrates in the littoral zone. The influence the choice of prey, but diffe­ bird species have different diet diversity, rent species may be differently affected and the quality of the prey species varies by the factors, depending on their greatly. In addition, different marine morphology, physiology or feeding birds have different feeding methods, methods. In many cases it is difficult to and ways of ingesting the prey. Some extract the effect of each of the factors, swallow the prey whole, while others because they may work in concert. only extract the organic content. The Introduction objective of this presentation is to show how different factors may influence the The marine habitats can roughly be decisions about prey choice among divided into open sea, shallow inshore marine birds. Various studies of birds waters and the littoral zone. Different feeding in the littoral and sub littoral bird species and groups exploit different zones from the northern temperate and feeding habitats and prey types. While Arctic areas are used as examples. most alcids and petrels forage out at Decisions about prey choice may be open sea, the cormorants, some alcids studied in different ways, and hypothe­ the terns, some gulls, and sea ducks are ses can be tested either qualitatively or feeding in inshore waters. The shore­ quantitatively by using optimality birds and many gulls feed in the littoral models. The examples both have used zone. In this paper I will discuss prey qualitative tests and optimality models choice in marine birds that feed in 2 inshore waters and littoral zones, by There is also an enormous vanat1on reviewing some studies from the north­ in the energy content of different marine ern temperate and Arctic areas. prey organisms. Fish consists mostly of protein and fat and very few inorganic Diets and feeding methods parts, while most molluscs (such as A comparison among different bivalves and gastropods) and echino­ marine bird species shows that they may derms, (urchins and sea stars) consist of have very different diets and also that the a large percentage of exoskeletons (shell, diet diversity within species varies tests) of little or no energetic value. One greatly. The common guillemot Uria gram of fish therefore gives much more aalge almost exclusively depend on a energy than one gram of urchin. few species of schooling fish. In the Barents Sea, the capelin is of major The differences in energy content importance for this species. After a may lead to the question of why not all collapse in the Barents Sea capelin marine bird species feed on high quality stock, some colonies of common prey such as fish. This question incorpo­ guillemots had a 80% population decline rates the evolution of life-histories in in one winter (Bakken & Mehlum, different bird groups, and is beyond the 1988). On the contrary at least 100 scope of this paper. However, the species have been recorded as prey of morphology of different birds obviously the common eider Somateria mollissima, sets limits to what they may feed on. mainly benthic invertebrates (e.g. Fish- and benthos specialists are very Cottam, 1939; Madsen, 1954; Goudie & different in shape, enabling them to Ankney, 1986; Bustnes & Erikstad, 1988 exploit the different resources effec­ and references therein) (Figure 1). tively. Most fish have great mobility, and

Diet diversity in marine birds

Echinoderms Molluscs Coelenterats Molluscs Polycheats Polycheats Polycheats Crustaceans Crustaceans Fish Fish Fish ,

Fig. I - Examples of diet diversity in different groups of marine birds. From left sea ducks (common eider) and gulls (herring gull), shorebirds (oystercatcher), inshore feeding alcids (Black guillemot) and cormorants, and finally ocean feeding alcids (common guillemot). 3

fish eating birds may use much energy to getic content, such as worms, crabs and find the fish at open sea and to catch it. shrimps, and they usually swallow the On the contrary, birds feeding on bottom prey whole (Cramp & Simmons, 1983; dwelling organisms exploit a resource Zwarts & Blomert, 1992). However, two that easily can be found in large quanti­ of 14 species of waders commonly found ties, which hardly moves and is easy to in NW Europe, the oystercatcher catch. Birds exploiting this resource, Haematopus ostralegus and the knot such as sea ducks, are bulk feeders and Calidris canutus are bivalve specialists. are not well designed for capturing fish, The oystercatcher often feeds on large even if they sometimes do. The fish blue mussels and cracks the mussel eating birds may be termed quality either by hammering through the shell or feeders while benthos feeders are by stabbing between the two valves, and quantity feeders. However, in between eating only the flesh (Crayford & Goss­ these extremes there are marine birds Custard, 1990 and references therein). with diets consisting of both fish and The knot is a specialist on Macoma benthos (e.g. gulls and to some extent baltica and other small clams, and cormorants). swallows the prey whole (Zwarts & Another important difference in Blomert, 1992). feeding method between groups of Gulls have a very diverse diet, but marine birds is that some dive for food littoral invertebrates are a central part of while others do not. Diving birds face the diet during much of the year (Cramp problems arising from a limited under­ & Simmons, 1983). Small items may be water time to catch prey, and must spend swallowed whole, while large items such time on the surface to recover the blood as urchins are either cracked open using gases between dives. In addition, diving the bill, or dropped from the air enabling is an energetically costly feeding method the birds to exploit organic tissue only (Butler & Jones, 1982; Ydenberg & (e.g. Irons et al 1986 and references Forbes, 1988; Ydenberg & , 1989). therein). Another important difference among Foraging theory marine birds is the way they ingest the A central concept m evolutionary prey. Diving birds usually swallow the biology is that organisms try to maxi­ prey whole. For fish feeding birds, it mise their Darwinian fitness, leaving as seems like an optimal solution because many descendants in future generations of the low inorganic content. However, as possible. Reproduction in species for a species that eat mussels and such as marine birds is an annual event urchins, most of the ingested material that only takes place in a restricted will be of no energetic value. Because of breeding season. In the period between this a sea duck like the common eider breeding seasons, the prime goal of the may ingest more than 2 kg of prey per birds is to survive, something which day, of which only a fraction is organic takes large amounts of energy. To get the (Bustnes & Erikstad, 1990; Guillemette, necessary energy may be a difficult task, 1994). especially for birds experiencing winters For non-diving species, the ingestion with low temperatures and reduced method varies. Shorebirds predominantly daylight. To survive such harsh condi­ feed on prey with relatively high ener- tions, marine birds must make feeding 4 decision based on costs and benefits of ses about cost and bendits or a certain different alternatives. In addition to behaviour. Different currencies might be describing all the diversity in diets we appropriate in different situations. With need a way to understand it. Foraging feeding behaviour the rate of food intake theory is an attempt to do so. is the currency in many studies. The Ultimately, cost and benefits of constraints are statements about the foraging decisions are measured in terms mechanisms of behaviour and the of fitness, but in most studies it is more physiological limitations of the animal. practical to measure it in more immedi­ A classical study showing how a ate ways such as energy expenditure or shorebird, the redshank Tringa totanus, energy intake (Stephens & Krebs, 1986; selected among various sizes of poly­ Krebs & Kacelnik, 1991). chaete worms Nereis diversicolor, was Studies have used different ways to carried out by Goss-Custard ( 1977). As analyse foraging decisions, including the availability of large worms in­ testing hypotheses by using both quali­ creased, the redshanks ate disproportio­ tative and quantitative predictions. If the nately more of them compared to small hypothesis that are maximising worms, and Goss-Custard was able to energy intake is tested, a typical qualita­ predict quantitatively the changes in the tive prediction would be that animals prey selection by using energy values of would select the most profitable prey small and large Nereis and their hand­ (that is the prey with highest relative ling times. energy content when other factors e.g. The first optimality models were handling time have been considered), simple rate maximising models, and they when exposed to several prey types in have been largely successful in explain­ equal amounts. A quantitative prediction ing animals foraging decisions in is more precise, based on cost-benefit relatively simple environments or experi­ relationships of selecting the different ments. However, models are becoming preys (e.g. energetic value of each prey more advanced, and account for other type, encounter rate, handling time). By factors that may influence feeding using such values, it would be possible decisions. One such factor is the risk of to predict the energy-maximising diet of predation, and numerous studies have the animal. If the prediction is in shown that animals sacrifice food intake accordance with the observed prey when facing potential danger from choice, one can be more confident that predators (Abrahams & Dill, 1989; the account of the animals foraging Krebs & Kacelnik, 199 1). decisions is correct. A more recent advancement in A main tool for making such analyses optimality theory is stochastic dynamic is optimality modelling. One advantage programming (Mange! & Clark, 1988). of optimal foraging models is that they The advantage of this technique is that it can give testable, quantitative predic­ is possible to analyse decision making in tions about foraging behaviour. That way a way that incorporates the state of the it is relatively easy to tell whether the animal (e.g. hunger level), and the hypotheses represented in the model are environmental stochasticity and trade­ right or wrong. Studies using optimality offs. The state of the animal changes models test hypotheses about currency dynamically as a result of its decisions, and constraints. Currencies are hypothe- which influences the optimal decisions 5 in a feedback loop (Krebs & Kacelnik, the depth and diving costs additionally 1991). constrain the birds. In risk sensitive models (variance Availability of different prey species sensitive), not only the average intake A factor that always will have large rate but also the associated variance influence on the prey choice of a influence foraging decisions (Caraco et predator is what can be found, or what is al 1990). Experimentally, it has been available. If profitable prey are rare, a shown that animals in poor condition forager will have to include less profit­ select the most variable of two choices able, but more common prey in the diet. with the same mean intake rate (e.g. Optimal foraging theory predicts that Caraco et al 1980). This is called 'risk animals should become more selective prone' foraging, and this tactic should be feeders as the availability of profitable chosen if the expected energy budget is prey increases (Irons et al 1986; Krebs & negative, because it will increase the Kacelnik, 1991). The reason for this lies survival probability. The mean intake in the 'principle of lost opportunity' will not give a positive energy budget, (Stephens & Krebs, 1986), which states but high returns from the variable source that if a profitable prey are abundant, the might. If the expected energy budget is opportunity to find profitable items is positive, the animal should select the lost if time is spent eating prey of lower least variable food source and be 'risk profitability (Krebs & Kacelnik, 1991). averse' (see Krebs & Kacelnik, 1991 for a review). Models of risk sensitivity are For many marine birds, the food state dependent, but differ from stochas­ situation change dramatically throughout tic dynamic models in that they do not the year, and the most profitable prey incorporate dynamic feedback between may only be found for a short time. A state and decisions. well known, but little studied example is the habit of sea ducks gathering at The approach spawning sites for fish, such as capelin, I will here review some studies of herring or lumpsuckers, to feed on fish marine birds that shows how different eggs (Cottam, 1939; Gj osceter & Scetre, factors influence the prey choice. Some 1974; Bustnes & Erikstad, 1988). During of these studies have used quantitative this time 25% of the diet of the common optimality models, but most have not. eider may consist fish eggs (Bustnes & Prey choice for marine birds when they Erikstad, 1988), and it is probably the can choose between different types of most energy rich food a sea duck ever food depends on various factors or encounters (fat and protein and no constraints such as the morphology, inorganic content). In pre-migration and physiology and internal state of the bird pre-breeding seasons it may be impor­ itself, and external factors such as prey tant. However, it might be of even availability, prey quality, predators and greater value to sea ducks during winter so on. The feeding environment of most darkness, and eiders in captivity in marine birds is very complex. For autumn strongly preferred lumpsucker example in the littoral zone, the extreme spawn when it was offered together with patchiness and the tidal cycle greatly blue mussel Mytilus edulis (Personal influence feeding decisions of the birds. observation). However, it is only For diving birds which feed on benthos, available in spring time, and then only for a short period of a few weeks. The 6 rest of the year other less profitable prey At neap low tides, only the upper littoral have to be eaten. In the common eider, zone is exposed, and here blue mussel blue mussels are the dominant prey in and barnacles are the available prey, most areas (Cottam, 1939; Madsen, which gulls also feed on. However, at 1954; Cramp & Simmons, 1977). Eiders spring tides the lower littoral zone is ex­ are distributed over a wide geographical posed, where gulls fed mainly on area from temperate Britain and France urchins, while the upper zone was (Maine in USA) to the high Arctic, and abandoned. A selection experiment also eiders are a species with very diverse showed that urchins were preferred prey diet. Over such a range, the benthic while mussels were not, the opposite to communities show large changes. In the what was found for eiders (see below). high Arctic, the blue mussel is absent Variation in profitability within prey and the eiders tend to feed on gastropods species and crustaceans (Weslawski & Skakuj , 1992). As stated above, the profitability of different prey species varies enormously, It has been established that blue but availability of profitable prey forces mussels have an relative energy density marine birds into eating less valuable twice as high as sea urchins Strongylo­ prey. Similar availability and profitabil­ centrotus droebachiensis, while the same ity relationships may be found within value for spider crabs Hyas aranesus is prey spectes. five times higher than for urchins (Guillemette et a/1992). It has also been The annual variation in the energy demonstrated that eiders show prefer­ content within littoral and sub littoral ence for mussels over urchins and select organisms is very high (Chambers & urchins at a lower rate than would be Milne, 1979; Zwarts & Wanink, 1993), expected by availability (Goudie & and may it also depend on where the Ankney, 1988; Guillemette et al 1992). organism grows, e.g. blue mussels from However, in a study area in Newfound­ the upper littoral have a much lower land with high urchin concentration, flesh content and heavier shells than more than 50% of the common eider diet those from the sub littoral, at the same consisted of urchins (Goudie & Ankney, length (Seed, 1976; 1979). Birds feeding 1986). Guillemette et al (1992) found on such organisms may increase their that crabs were a preferred food item, energy intake several times, by selecting but overall it only made up a very small the right habitats or sizes of prey. fraction of the diet, because it had such Especially for birds that swallow the low availability (see below). organisms whole, such as eiders and knots, the gain from being selective is An example of a bird species feeding high. Bustnes & Erikstad (1990) found on the same species as the common eider that common eiders wintering in nor­ is the glaucous-winged gull Larus thern Norway fed on small mussels (14 glaucescens in Alaska. It feeds in the mm), and thereby reduced the daily littoral zone at low tide, and by far the intake of shell by 1 kg compared to most commonly selected prey item are feeding on 40 mm mussels. However, urchins, followed by blue mussels (Irons there is no consistent size selection et al 1986). However, the level of tides among mussels by eiders, and in its constantly changes and prey availability southern distribution range, eiders feed is different at neap and spring low tides. on mussels of about 40 mm (e.g. Madsen 7

1954; Nehls, 1995). Mussels in southern best compromise knot eat medium sized areas where temperatures are higher, Macoma (Zwarts & Blomert, 1992). grow faster and have relatively lighter Feeding methods and digestive shells at the same length compared to constraints mussels from northern areas (Seed, 197 6). Large mussels are therefore Sea ducks, gulls and shorebirds relatively more profitable in the south generally feed on the same types of prey, than in the north. The hypothesis that that is molluscs, echinoderms, crusta­ eiders try to minimise the intake of ceans and polycheates, but the studies inorganic parts when choosing among described above indicate that different different sizes of mussels was supported species of birds prefer different prey. by an experiment showing that eiders Why for example do gulls prefer urchins avoid littoral mussels with heavy shell while eiders do not? A factor that may and prefer sub littoral mussels of the provide an answer is the feeding meth­ same size (Bustnes in prep). Nehls ods of the different bird species, which is ( 1995) found that eiders in the Wadden a result of their morphology. The Sea changed their size selection in different groups of bird species are course of the winter, from eating large facing different constraints when mussels in January and smaller ones in ingestion and digestion are concerned. June. This corresponds well with the Sea ducks swallow items whole and mussel spawning. That is large repro­ process it through the gut (Guillemette, ductive mature mussels spawn much of 1994). Gulls on the contrary either peck their organic content in spring making it out the flesh of the prey or swallow it more profitable to feed on small non whole, but do not process the inorganic mature ones (Zandee et al 1980; Lowe et parts in the gut since they are able to a/1982; Zwarts & Wanink, 1993). regurgitate (e.g. Irons et al, 1986). Most shorebirds eat worms crabs or shrimps Several studies have shown that that are swallowed, and do not regurgi­ shorebirds select the energetically most tate inorganic parts of the prey (Zwarts profitable size classes of prey (reviewed & Blomert, 1992). The oystercatcher, by Cayford & Goss-Custard, 1990), and however, open the bivalves and ingest in the oystercatcher, this meant a change the flesh only, while the knot swallow of sizes from 50 mm blue mussels in the bivalves whole (Zwarts & Blomert, early winter to 25-30 mm after mussel 1992). Recent studies indicate that the spawning, in spring (Cayford & Goss­ limiting factor in the food processing of Custard, 1990). both common eiders, knots and whim­ For the Macoma baltica feeding knot brei is the digestive capacity of the gut eating thin-shelled individuals would be (Zwarts & Dirksen, 1990; Zwarts & highly profitable. However, Macoma is Blomert, 1992; Guillemette, 1994). buried in the mud and the birds have to Common eiders can ingest mussels two probe with the bill, but they cannot reach times faster than they can assimilate deeper than 2-3 cm. The shell thickness energy in the gut (Guillemette, 1994). of Macoma varies with burying depth, This means that these species are much and close to the surface the they are more constrained by the flesh/shell thick-shelled, while the thin-shelled ones (organic/inorganic) ratio, than gulls and are found deeper than the reach of the oystercatchers that only assimilate the knot, and are not accessible. As the a mussel or urchin tissue. Even if the 8 organic/inorganic ratio should be means that they have a restricted time to important for them too, because of search for prey. At the same time diving search and handling times, they may is a energetically costly feeding mode, benefit from taking other prey types or involving depletion of blood and muscle sizes, e.g. the largest prey they can open. oxygen, and recovery times at the surface (Butler & Jones, 1982; Ydenberg Time constraints & Forbes, 1988; Ydenberg & Cl ark, Prey choice is influenced by the time 1989). available for feeding (Plowright & Beauchamp et al ( 1992) modelled Shettleworth, 1991). An example of a how diving duration and depth would time constraint is the effect that reduced influence the prey selection in common day length has for diurnal foraging eiders, using dynamic programming (see species wintering in northern areas. Sea Mange! & Clark, 1988). ducks are predominantly daytime feeders, but in their northern wintering In the Gulf of St. Lawrence wintering areas, the daylight, and thereby foraging common eiders feed in various benthic time may be reduced to 4-5 hours in mid habitats and in one type, the Argarum winter compared to 20 hours in spring zone, they mainly feed on two prey (Systad, 1996). In such situations, Systad types, ubiquitous but low energetic ( 1996) showed that common eiders and urchins and high energetic but rare long-tailed ducks used proportionately spider crabs, that are brought to the more time for feeding when days were surface and swallowed (Guillemette et short compared to long days. al, 1992; Beauchamp et al, 1992). Their model showed that encountered crabs For shorebirds that feed in the littoral should always be accepted while urchins zone, the problem with tidal periods also should not be accepted before late in the causes feeding time shortage because at dive and it also predicted that whether an high tide they are prevented from eider should accept an urchin depends on reaching the feeding sites. Swennen et al diving depth, dive duration and the stage (1989) constrained the feeding time of of the actual feeding bout. First, urchins captive oystercatchers. The experiments should be accepted earlier in shallow simulated a natural situation where the than in deep water because the energy length of low tides are both predictable and time expenditure and thereby the and unpredictable (e.g. due to bad cost of a dive, increases with depth. That weather). They found that the birds is, eiders are more selective when increased intake rates as the time feeding at deep water. Secondly, the available was reduced, by spending birds are more likely to accept an urchin proportionately more time feeding as the amount of energy accumulated during shorter tides, and by reducing increases, especially if much energy has search and handling time. However, the been found early in a feeding bout. This birds only fed on one type of prey, and comes from the fact that the need for did not actively select among different selectivity is lower as they reach the sizes of prey. energetic goal of the feeding bout. A time constraint of particular Thirdly, when feeding in deep water interest for prey selection are the choosiness increases as time proceed in a problems faced by diving species. feeding bout, while it decreases in Diving animals can only stay in their shallow water. In general, urchins should feeding for a short time, and this 9 be rejected in early dive stages as a that eiders used three habitat types; kelp consequence of the high profitability of beds, urchin barrens and Agarum zones. crabs, which are always accepted when These habitats had large differences in encountered, while urchins are taken the occurrence of different prey types. In later in the dives when the cost of kelp beds eiders fed on blue mussel, rejection increases, because of the high while in Agarum zones they fed on the energy costs of diving and the danger of profitable but rare spider crabs, and fruitless dives. urchins. Agarum zones and kelp beds The test of this model with field data had about the same average energy showed that it predicted well the prey return, but the variation in energy return that common eiders brought to the between kelp beds and Agarum zones surface when feeding in shallow water, was large, being greater in the latter (the but it did not do so well for deep water energy return from urchin barrens was feeding birds. There may be several much lower). They further observed that reasons for this result, such as underes­ eiders fed in large flocks or small flocks, timation of diving costs. However, it and that mostly small flocks fed in the may that eiders swallow some smaller Agarum zones. It turned out that the prey under water when diving deep, individuals in small flocks were in poor which the observer would be unable to condition. The interpretation of the see. This is one of the few attempt to behavioural pattern was that birds in solve the prey selection as a dynamic poor condition were searching for rare problem, involving different prey types but high quality prey, thereby increasing and different diving depths. their survival changes since they may have had a negative energy budget if Risk-sensitivity they did not employ the variability tn As state above, risk sensitivity refers energy return in the Agarum zone. to variance associated with foraging Risk of predation decisions (Caraco et al, 1980, Ha et al, 1990). Prey- or habitat selection should The risk of being killed by predators be influenced by the probability of a has been found to influence the choice of energy shortfall. If a predator expects to feeding site and prey of animals (see have a negative energy budget it should Krebs & Kacelnik, 1991 for a review). If behave in a risk prone way, and select the best prey are found at a site where prey or habitats with high variance the animal is being very exposed and (Krebs & Kaclenik, 1991). Risk prone cannot take cover, the chances of being behaviour is to be expected among killed by a predator increases. It may animals in poor condition, where such a thus pay to stay in cover and feed on less strategy will be the best option in terms energetic profitable prey or stay in less of survival. profitable patches. That animals react to the presence of predators by selecting Again the study of wintering common prey or feeding sites with lower energy eider study in the Gulf of St. Lawrence return, has been shown in great tits by Guillemette and colleagues, provide (Krebs, 1980), ground squirrel (Newman an example. The authors interpreted the & Caraco, 1987), and in several fish exploitation of the different habitat and (Dill, 1987). prey by the common eiders in a risk sensitive way, using a qualitative model Both sea ducks and waders are (Guillemette et al, 1992). They observed exposed to predation from raptors 10

(Bijlsma, 1990). For shorebirds feeding small food items which can be swal­ on mudflats, staying far out may mean lowed under water, but which probably that they are less protected compared to give less energy intake. This idea feeding close to the shore. I they forage remains to be tested. Schenkeveld & close to the shore, the prey availability Y denberg ( 1985) found that surf seaters and quality would be different (e.g. M elanitta perspicillata that were degree of air exposure of mussels). From harassed by glaucous-winged gulls this it is expected that risk of predation showed higher diving synchrony than will affect the patch and prey selection when there were no gulls. Especially of these species. I know of no study that pronounced was the effect on surfacing shows how prey selection may be altered synchrony. That is, some birds curtail in marine birds, but in turnstones it has their dives to be able to surface with the been shown that in the premigratory rest of the group to dilute the risk of phase, when the need for accumulating kleptoparasitism. Schenkeveld & body reserves is high, the birds are less Y denberg concluded that such behaviour vigilant and feed more. This seems to be would have an effect on the average a change in the optimal behaviour, and quality of the prey captured, because the the benefits of increased resource search time during the dive must be accumulation outweigh the additional shortened. Kleptoparasites therefore risk of predation (Metcalfe & Furness, impose two costs on the seaters; prey are 1984) stolen and less profitable prey have to be accepted. Kleptoparasitism Another problem for many seabirds, Risk of ingesting parasites shorebirds (Hesp & Barnard, 1989 and Very few studies have considered the references therein) and sea ducks idea that risk of ingesting parasites (Ingolfson, 1 964) is that gulls and skuas should prevent marine birds from eating may steal their food items, so-called the prey that gives the highest energy kleptoparasitism (Furness, 1987). Being intake. The invertebrates of the littoral harassed by a kleptoparasite means that zone are often very heavily parasitised energy intake rate will be lower, both by various helminths, and many of these because costly food items are lost, and parasites may have very pathogenic because of the interruption in feeding effects on their hosts (Galaktionov & activity. Lapwings Vanellus vanellus, Bustnes, 1996 and references therein). If respond to kleptoparasites by moving prey are infected it may not be very wise away from gull landing near them (Hesp to eat them even if the energy content is & Barnard, 1989). If possible, selecting high. It has been shown by Hulscher smaller-, easy-handled-, but less ener­ (1982) that oystercatchers rejected getic prey, that cannot be stolen may be Macoma baltica that were heavily beneficial under heavy kleptoparasitism. infected with the trematode Parvatrema Sea ducks are vulnerable, because affinis. This indicates that parasites may they dive and as they arrive on the be a factor that could reduce the energy surface gulls steal their food (Ingolfson, intake rate of waders. 1964). Large items such as crabs and In common eiders there have to my urchins have to be brought to the surface knowledge been no studies of how and in cases where the rate of klepto­ parasite infections influence prey choice. is high it may pay to choose However, it is interesting to note that the 11 most common prey, the blue mussel has eiders, is that it shows how it is possible very low levels of parasite infections to understand more of foraging behav­ (Meire & Ervynck, 1986). In contrast, iour by using different types of models. the shore crab is the Long term field studies are also very intermediate host for one of the most important, for example those of wading pathogen parasites of eiders, the acan­ birds such as the oystercatcher, on which thocephalan Profilicollis botulus several research groups have been (Garden et al, 1964; Thompson, 1985). working for decades. However, the eider In other words if the common eiders in case is actually one of the first studies of poor body condition start to feed on high sea ducks that use recent advances in energy shore crabs to increase survival, foraging theory to understand the as suggested by Guillemette et al (1992), foraging behaviour. By simply looking at they may suffer an additional risk of prey availability and prey choice one ingesting pathogenic parasites, compared would probably find qualitative support to those that mostly fed on mussels for the hypothesis that the occurrence (Figure 2). and energetic value of different preys (mussels, urchins and crabs) accounted Discussion for the prey selection of eiders. Perhaps In this review I have made several it would also be possible to make a rate­ references to the study be Guillemette maximising model with quantitative and colleagues on wintering common predictions that would account for the eiders in the Gulf of St. Lawrence observed prey choice overall in the (Guillemette et al, 1992, Beauchamp et population. However, by looking at the al, 1992, Guillemette, 1994) . The reason feeding habitats (kelp beds, urchin for this, apart from my own interest in barrens, Agarum zones) of different indi-

The risk of ingesting parasites

·.

High energy, but dangerous parasites (P. botulus)

Intermediate energy, but many potentially dangerous trematodes , Intermediate energy, and few parasites

Low energy, but few parasites

Fig. 2 - Energy content and parasites of different prey for the common eider. From top; crab, periwinkle, blue mussel and sea urchin. 12 victuals the authors were able to show birds do not necessarily select an energy­ that the body condition of the birds maximising diet is a study by John Ball influenced their foraging decisions, and (Ball, 1994) on canvasbacks, a freshwa­ they were either risk prone or risk ter diving duck. He was able to produce averse. They were further able to predict an experimental situation that approxi­ much of the prey selection of birds mated the problems of prey choice in feeding in the Agarum zones (presum­ real-world condition, where the birds ably those in poor condition) by using a chose between various prey of different dynamic model that incorporated dive profitability. In this environment there duration and depth. What this study was no danger of predation or variation demonstrates is that no model, and no in state of the birds that would confound single factor will account for the whole the results, so the birds would be process of prey selection in a population. expected to maximise energy intake. He Individuals will have different optimal also made an optimality model that strategies depending on their situation. incorporated several different factors The factors that I have mentioned do (prey depletion, feeding rates and by no means exclude each other, and digestion rates) from which he predicted they may often work in concert. It is the energy-maximising diet. The result therefore difficult to find the effect on was that the birds did not consume prey prey choice of each of them. For birds in the proportion predicted by the model. feeding in environments as complex as It seemed as if canvasbacks when facing littoral- and sub littoral zones, the habi­ a complex foraging decisions were using tats are extremely variable over short simple «rules of thumb» to guide their distances in terms of prey density and behaviour. First the bird may use taste quality, habitat patchiness, water depth, cues to evaluate prey profitability, and tidal cycles, occurrence of predators, then select the most profitable prey. conspecific competitors, parasite bur­ Second, if taste cannot be used take the dens, and others. All these factors makes larger prey, and thirdly if prey vary in it very hard for a bird to select a diet that texture, take the softer prey that will be maximises any currency, because all the easier to digest. The canvasback is a necessary information about the environ­ duck that face similar complex environ­ ment is unlikely to be available. ments as many marine birds, both sea ducks, gulls and shorebirds. It is there­ The idea that animals try to maximise fore reason to believe that similar mis­ the average rate of energy intake has matches between model and real world been very helpful in understanding how situations will be found as more tests of animals select their prey, but it is also optimality models are conducted on clear that there is a lot of variation in this different marine birds, and perhaps system that cannot be explained by such "rules of thumb" in many cases can simple models. Studies and reviews have better explain foraging behaviour. found that rate-maximising models make good predictions of the diets in two-prey Acknowledgement choice cases, but the predictive power of I wish to thank Dr. Ron Y denberg for this theory decreases in a complex very valuable comments on an earlier multifood systems (Schluter, 1981; draft of the manuscripts and for correct­ Ward, 1993; Ball, 1994). One of the ing the English. more recent studies showing that diving 13

References Abrahams M, Dill L. A determinant of the . pus ostralegus: an optimality approach. energetic equivalence of the risk of preda­ Anim Behav 1990; 40: 609-24 tion. Ecology 1989; 70: 999-1 007 Chambers MR, Milne H. Seasonal variation Bakken V, Mehlum F. AKUP sluttrapport in the condition of some intertidal inverte­ sj ofuglundersokelser nord for 74° NI Bj0rn- brates of the Ythan Estuary, Scotland. Estuar 0ya. Norsk Polarinst Rap Ser No. 44, 1988 Coast Mar Sci 1979; 8: 411-9 Ball JP. Prey choice of omnivorous canvas­ Cottam C. Food habits of North American backs: imperfectly optimal ducks? Oikos diving ducks. US Dep Agric Tech Bull No 1994; 70: 233-44 643, 1939 Beauchamp G, Guillemette M, Ydenberg RC. Cramp S, Simmons KEL. Handbook of the Prey selection while diving by Common birds of Europe the Middle East and North Eiders, Somateria mollissima. Anim Behav Africa. The birds of the Western Palearctic. 1992; 44: 417-26 Vol I. Oxford University Press, 1977 Bijlsma RG. Predation by large falcons on Cramp S, Simmons KEL. Handbook of the wintering waders on the Banc D'Argu in, birds of Europe the Middle East and North Mauritanins. Ardea 1990; 78: 75-82 Africa. The birds of the Western Palearctic. Vol Ill. Oxford University Press, 1983 Bustnes JO, Erikstad KE. The diets of sympatric wintering populations of Common Dill LM. Animal decision making and its Eider Somateria mollisma and King Eider S. ecological consequences: the future of spectabilis in northern Norway. Ornis aquatic ecology and behaviour. Can J Zoo! Fennica 1988; 65: 163-8 1987; 803- 11 Bustnes JO, Erikstad KE. Size selection of Furness RW. Kleptoparasitism in seabirds. common mussels Mytilus edulis by common In: Croxall JP, ed. Seabirds; feeding ecology eiders Somateria mollissima: energy in marine ecosystems. Cambridge: Cam­ maximization or shell weight minimization. bridge University Press, 1987 Can J Zoo! 1990; 68: 2280-3 Galaktionov K, Bustnes JO. Diversity and Butler PJ, Jones DR. Comparative physiol­ prevalence of seabird parasites in intertidal ogy of diving vertebrates. In: Lowenstein OE, zones of the southern Barents Sea coast. ed. Advances in physiology and biochemis­ NINA-NIKU Project report no. 004, 1996 try. New York: Acad. Press, 1982: 179-364 Garden EA, Rayski C, Thorn V. A parasitic Caraco T, Martindale S, Whittam TS . An disease in eider ducks. Bird Study 1964; 11: empirical demonstration of risk-sensitive 280-7 foraging preferences. Anim Behav 1980; 28: Gj osceter J, Scetre R. Predation of eggs of 820-30 Capelin (Mallotus villosus) by diving ducks. Caraco T, Blanckenhorn WU, Gregory GM, Astarte 1974; 7: 83-9 Newman JA, Recer GM. Risk-sensitivity: Goss-Custard JD. Optimal foraging and the ambient temperature affects foraging choice. size-selection of worms by redshank Tringa Anim Behav 1990; 39: 338-45 totanus in the field. Anim Behav 1977; 25 : Cayford JT, Goss-Custard JD. Seasonal 10-29 changes in the size selection of mussels, Mytilus edulis, by oystercatchers, Haemato 14

Goudie RI, Ankney CD. Body size, activity Lowe DM, Moore MN, Baync BL. Aspects budgets, and diets of sea ducks wintering in of gametogenesis in the marine mussel, Newfoundland. Ecology 1986; 67: 1475-82 Mytilus edulis L. J Mar Bioi Assoc UK 1982; 62: 133-45 Goudie RI, Ankney CD. Patterns of habitat use by sea ducks wintering in southeastern Madsen JF. On the food habits of the diving Newfoundland. Ornis Scand 1988; 19: 249- ducks in Denmark. Dan Rev Game Bioi 56 1954; 2: 157-266 Guillemette M. Digestive-rate constraint in Mange! M, Clark CW. Dynamic program­ wintering common eiders (Somateria mollis­ ming in behavioural ecology. Princeton: sima): implications for flying capabilities. Princeton University Press, 1988 Auk 1994; Ill: 900-9 Meire PM, Ervynck A. Are oystercatchers Guillemette M, Y denberg RC, Himmelman (Haematopus ostralegus) selecting the most JH. The role of energy intake in prey and profitable mussels (Mytilus edulis)? Anim habitat selection of Common Eiders Somate­ Behav 1986; 34: 1427-35 ria mollissima in winter: a risk-sensitive Metcalfe NB, Furness RW. Changing interpretation. J Anim Ecol 1992; 61: 599- priorities: the effect of pre-migratory 610 fattening on the trade-off between foraging Ha JC, Lehner PN, Farley SD. Risk-prone and vigilance. Behav Ecol Sociobiol 1984; foraging behaviour in captive grey jays 15: 203-6 Perisoreus canadensis. Anim Behav 1990; Newman JA, Caraco T. Foraging predation 39: 91-6 hazard, and patch use in grey squirrels. Anim Hesp LS, Barnard CJ. Gulls and plovers: age­ Behav 1987; 35: 1804- 13 related differences in kleptoparasitism among Nehls G. Strategien der Ernahrung und ihre black-headed gulls (Larus ridibundus). Bedeutung fiir Energiehaushalt und Okologie Behav Ecol Sociobiol 1989; 24: 297-304 der Eiderente (Somateria mollissima) (L., Hulscher JB. The oystercatcher as a predator 1958). University of Kiel, 1995 of the bivalve, Macoma balthica in the Dutch Plowright CMS, Shettleworth SJ. Time Wadden Sea. Ardea 1982; 70: 89-152 horizon and choice by pigeons in a prey Ingolfson, A. Behaviour of gulls robbing selection task. Anim Learn Behav 1991; 19: eiders. Bird Study 1964; 16: 45-52 103-12 Irons DB, Anthony RG, Estes JA. Foraging Seed R. Ecology. In: Bayne BL, ed. Marine strategies of glaucous-winged gulls in a rocky Mussels. Cambridge: Cambridge University intertidal community. Ecology 1986; 67: Press, 1976: 13-65 1460-74 Seed R. Variation in the shell-flesh relation­ Krebs JR. 1980. Optimal foraging, predation ships of Mytilus: the value of sea mussels as risk and territory defence. Ardea 1980; 68: items of prey. Veliger 1979; 22: 219-21 83-90 Schenkeveld LE, Y denberg RC. Synchronous Krebs JR, Kaclenik A. Decision making. In: diving by surf seater flocks. Can J Zoo! Krebs JR, Davies NB, eds. Behavioural 1985; 63: 25 1 6-9 ecology. An evolutionary approach. Oxford: Schluter D. Does the theory of optimal diets Blackwell Scientific Publications, 1991: 105- apply in complex environments? Am Nat 36 1981; 118: 139-47 15

Stephens DW, Krebs JR. Foraging theory. Zwarts L, Blomert AM. Why knot Calidris Princeton: Princeton University Press, 1986 canutus take medium-seized Macoma balth­ ica when six prey species are available. Mar Swennen C, Leopold MF, De Bruun LLM. Ecol Prog Ser 1992; 83: 113-128 Time-stressed oystercatchers, Haematopus ostralegus, can increase their intake rate. Zwarts L, Wanink JH. How the food supply Anim Behav 1989; 38: 8-22 harvestable by waders in the Wadden Sea depends on the variation in energy density, Systad G. Effects of reduced day length on body weight, biomass, burying depth and the activity pattern of wintering sea ducks. behaviour of tidal invertebrates. Netherlands Cand Scient thesis. University of Troms�<'l, JSea Res 1993; 31: 44 1 -76 1996 Thompson AB. Transmission dynamics of Profilicollis botulus (Acanthocephala) from crabs (Caracinus maenas) to eider ducks (Somateria mollissima) on the Ythan Estuary, N.E. Scotland. J Anim Ecol 1985; 54: 605-16 Ward D. Foraging theory, like all other fields of science needs multiple working hypothe­ ses. Oikos 1993; 67: 376-8 Weslawski JM, Skakuj M. Summer feeding of seabirds in Tkahaia Bay, Frans Josef Land. In: Gjertz I, M0rkved B, eds. Environmental studies from Frans Josef Land, with emphasis on Tikhaia Bay, Hooker Island. Norsk Polarinst Meddelelser no. 120, 1992: 55-62 Y denberg RC, Forbes LS. Diving and foraging in western grebe. Ornis Scand 1988; 19: 129-33 Ydenberg RC, Clark CW. Aerobiosis and anaerobiosis during diving by western grebes: an optimal foraging approach. J Theor Bioi 1989; 139: 437-49 Zandee DI, Kluytmans JH, Zurburg W, Preter H. Seasonal variations in the biochemical composition of Mytilus edulis with reference to energy metabolism and gametogenesis. Neth J Sea Res 1980; 14: 1-29 Zwarts L, Dirksen S. Digestive bottleneck limits the increase in food intake of whim­ breis preparing for spring migration from the Banc D'Arguin, Mauritania. Ardea 1990; 78: 257-78 Bull Scand Sac Parasitol 1996; 6 (2): 16-30

NEMATODE PARASITES OF MARINE- AND SHORE BIRDS, AND THEIR ROLE AS PATHOGENS

Bans-Peter Fagerholm Institute of Parasitology, Deptartment of Biology, Abo Akademi University, BioCity, 20520 Abo, Finland

Introduction

Parasitic organisms constitute semi­ Among the enopleans, two parasitic integrated components of the host animals groups are found, the supeifamilies and they often have a longstanding co­ Trichinelloidea (Capillariinae) and Dioc­ phylogenetic history. Studies of birds on tophymatoidea (Eustrongylidae), species aspects of parasite-host interactions in the of both of which occur also in coastal case of nematode parasites, bound to birds. The remaining enoplean groups aquatic biotopes, are scarce. One reason include predominantly free living aquatic for this has often been a diagnostic organisms. The Rhabditea contains the problem. Today new methods have made main part of the parasitic forms including the species determination of parasitic those which occur as parasites in coastal nematodes feasible even in groups which birds. These are mainly found among the traditionally have been difficult. In Rhabditoidea, Strongyloidea, Ascari­ addition to better optical- and electron doidea, and within the Spirurida among microscopes, biochemical methods, the Dracunculoidea, Thelazioidea, Ha­ including isoenzyme electrophoresis and bronematoidea, Acuarioidea, Diplo­ DNA based applications, provide better triaenoidea, Aproctoidea and Filari­ tools for such work. However, it is oidea. apparent that more basic investigations Nematodes may be encountered in dealing with the definition of parasite almost any organ of the birds. The most populations, and possible sympatric and commonly parasitized site is the allopatric sibling forms, are needed. gastrointestinal tract, the proventriculus Based on structural features the and gizzard in particular, and its adjacent Phylum Nematoda has been divided into dermal layers. They may be found in the two classes: Enoplea (Aphasmida) and skin, the heart, in the lungs etz. The Rhabditea (Phasmida). (See Adamson, species of different systematic groups 1987). The classification of parasitic generally have their specific predilection nematodes of vertebrates was critically sites. analysed by Anderson et al (eds) (1974- Because there still are rather few 1983) in the by now classic CIH Keys to studies made on the pathogenicity of nematode parasites. 17 nematodes in wild birds, one may have (1994). There are in addition numerous the perception that nematodes rarely faunistic studies made. cause diseases in birds. Furthermore, the The present review points at the large impact of a nematode infection on a bird diversity of nematodes which live as community is difficult to assess and parasites in marine- and shore birds and evidently demands extensive investiga­ discusses, in some cases, their effect on tions. Results available on the effects of the bird host, or the bird community. certain nematodes on bird communities suggest that the parasite may, in �ddition ENOPLEA of being a disease agent, secondanly also Trichinelloidea: The capillarids (Capil­ modify the reproductive behavior and larinae) are common parasites in different other behavioral features of the bird. The vertebrates including coastal birds interesting results by Hamilton & Zuk (Madsen, 1945). In birds they occur in the (1982) suggest a positive relation betw en � gastrointestinal canal and the oes phagus parasites, including one nematode spectes, � (Barus et al., 1978). These parasttes are and "striking display", in male and female thin (0.05 mm) nematodes, females attain­ birds (North American passerines) assur­ ing lengths of 20-40 mm. The �ife-cy�le is ing genetic disease resistance in the direct or includes an intermediate sot! (or offspring. It is further evident that h�man aquatic?) annelid. Autoinfection is known activities may locally upset estabhshed to occur in Capillaria philippienensis, a dynamics of parasite population p ttems, � zoonotic species (Cross & Basca-Sevilla, for example by drastically affectmg t�e 1983; Cross, 1992). In the palaearctic size of final-, intermediate- or paratemc region numerous species of the g nus host populations. � have been recorded in coastal birds, This presentation is largely based on particularly in species associated with the nematode classification adopted in the fresh- or brackish water sites. Based on CIH-keys on nematode parasite (Ander­ certain structural criteria, the son et a!, eds, 1974-1983). In addition to Capillaria has in recent studies been split primary papers the extensive monograph into numerous entities (Moravec, 1982, by McDonald ( 1969), and the one ?Y 1987; Moravec et al., 1987; Barus & Barus et a! ( 1978) contain data on parasite Sergejeva, 1989a,b, 1990). biology and host species and give references to early studies. References to Dioctophymatoidea: Species of the early published data on pathological family Eustrongylides Jagerskiold, 19�9 effects of nematodes in shore birds are are dioctophymatoidean worms found m found in these monographs. The life­ the proventricular wall of piscivorous cycles of nematode parasites have been birds. Karmanova ( 1968) and Measures summarized by Anderson (1992). Some (1987a,b, 1988a) studied the biology of recent faunistic, systematic and biogeo­ this group. The life cycle of Eustrongy­ graphic studies include those by Bakke & lides includes a freshwater tubificid and Barus (1975, 1976), Wong & Anderson fish as vector organisms (Karmanova, (1993), Anderson & Wong (1996), 1965, 1968; Lichtenfels & Stroup, 1985). Hoberg (1996), Skimisson & Jonsson The adult worms are found in the wall of (1996) and Olafsdottir et a! (1996). See the proventriculus of piscivorous birds also Borgarenko (1990), Wong (1990), where they form marked tumourlike Bychova (1991), Okulewicz & Koubek structures. Eustrongylides spp. have been experimentally found to develop in the EMO

RAAMATI ik'(JG! I ------·-·-·-·-· ·-··· --·--- -··

18

proventricular wall of numerous patent period was observed to be 16-24 piSCivorous and anatid birds (see days p.i. (Sprinkle, 1973). In established Measures, 1987b), It was also found to worms, the anterior end, and the tail, are develop (100% prevalence; own data) in actively protruded through separately domestic chicken (Fagerholm, 1979) formed distinct orifices into the contrary to observations by Brand & proventricular lumen from which food Cullinan ( 1943). The genus was revised material is obtained, and into which eggs by Measures (1988b). Three species out are released (own data). of the numerous species reported in the Locke et al ( 1966) found Eustrongy­ literature were considered valid: E. lides to cause a merganser "die-off' due ignotus, JagerskiOld, 1909 is a species to extensive migration of larvae causing occurring in Ardea, Ciconiiformes and massive tissue destruction and hemor­ from U.S.A. (Florida), rhage, particularly in the liver. The Brasil and New Zealand); E. excisius authors also referred to a few earlier Jagerskiold, 1909 occurs in Pelecani­ repmts. Wiese et a! (1977) found the formes, Ciconiiformes, Anseriformes in highest mortality in nestlings in ardeids Europe, former U.S.S.R., Taiwan, India, due to E. ignotus infection. Roffe ( 1988) Australia, Middle East; E. tubifex found severe inflammation in the (Nitzsch in Rud., 1809) (see Fastzkie & peritoneum caused by Eustrongylides Crites, 1977) occurs in Gaviiformes, causing the death of 400 common egrets. Anseriformes, Ciconiiformes, Podicipe­ Spalding & Forrester (1993a) found the diformes from Europe, former U.S.S.R., severity of disease to be inversely related Brazil., U.S.A., Canada. to the age of the birds, and directly related Observations on Eustrongylides in fish to the number of parasites. They found in northern Europe, where large sized the infection to result in emaciation, and, larvae often are found in salmonid fish probably, traumatic death. In the inter­ (Kennedy & Lie, 1976; Kennedy pers. mediate host larvae may migrate to fish comm.) measuring 90 mm in length (own muscle if the fish is not properly stored data from farmed rainbow trout ( Oncho­ ( et al, 1978). Larvae have once rhynchus mykis) in Norway) and small been recorded in muscle of cultivated larvae (length less than 40 mm) is present rainbow trout fed feral fish in E. Finland mainly in percid fishes (Fagerholm, 1979, (own data). 1982), suggesting that there might be an Eustrongylides-1arvae are in addition additional species present in the European known to cause extensive damage and region, the taxonomic position of which death in abnormal hosts. Berland (196 1) remains to be settled. found a few corvids to have died from Notes on disease: The larvae enter the ingestion of fish infected with larvae. In tissues primarily trough compound gland an attempt to infect laboratory hamsters lobules of the proventriculus of the birds. (n=4), from Acerina cernua, with ten Fibrous capsules are present already two larvae each, within 24h all animals days after infection (p.i.) (Measures, behaved abnormally and one had died, 1987b). They migrate into the tunica while, when farmed mink (Mustela muscularis and remains inside a connec­ mustela) was infected (n=IO) by stomach tive tissue capsule. Large numbers of tube, no worms were subsequently found macrophages, heterophils and giant cells (own data). Shirazian et a! (1984) studied are seen in histological sections in the the effect of similar worms in the rabbit. affected tissue (Measures, 1987b). The E. excisus was found to produce eggs in a 19 sturgeon, serving as accidental definitive americanum, H. bronchia/is (syn H. host (Michailov et al, 1992). Accidental brantae & C. bronchia/is)) in Finland infection in man, by eating raw infected with a total prevalence of 0.5% in 3000 fish resulted, in surgical intervention due birds studied. See also Simpson & Harris to long ranged migration of larvae. The (1992). infection was due to customers in a bar Notes on disease: These nematodes, eating small feral fish introduced by the commonly named gape worms, occur in owner to an aquarium from a nearby pond the trachea of numerous birds. They are (Perry, 1982). Some additional human reported world-wide (McDonald 1969), cases have also been recorded. as a serious disease factor and are known Muspiceoidea: This heterogenous to cause respiratory distress in birds superfamily has an uncertain systematic (including emaciation, anaemia, and position among the Enoplea. Robert­ mortality) (Soulsby, 1986). Watters dollfusidae (Robertdollfusa Chaboud & (1994) and So veri et al (1989) diagnosed Campana, 1950) are found in tissue of respiratory distress due to Cyathostoma some birds, including Falconidae. and Howorkonema-infections, while Zieris & Betke (1991) observed Cyatho­ RHABDITEA stoma to cause mortality m Aix Rhabditoidea: Out of a few strongyloidid galericulata. (Strongyloididae) species reported from Trichostrongyloidea: Of the Amidosto­ birds one, Strongyloides turkmenicus matidae a few species of the genus Kurtieva, 1953, has been recorded in a Amidostomum are common parasites coastal bird (Larus canus) (Bakke & mainly of anseriform birds. They are Barus, 1976). found under the lining of the gizzard, and Strongyloidea: Strongylid parasites in particular at the junction of the occurring in coastal birds belong to the proventriculus and duodenum. (Species: family Syngamidae. This is a very small A. acutum (Lundahl, 1848), A. anseris group compared with other families (Zeder, 1800), A. fulicae (Rud., 1819), A. which manly are parasites of different spatulatum Baylis, 1932). The same site mammals. However, the is not is inhabited by the single species of the settled. Included are three genera: Trichostrongylidae, Epomidostomum un­ cinatum (Lundahl, 1848). Generally these a. Syngamus Siebold, 1836; parasites are noted to have a direct life b. Cyathostoma (Cyathostoma) (Elan­ cycle, although paratenic hosts have been chard, 1849); reported. c. Cyathostoma (Hovorkonema) Ture­ Notes on disease: In numerous early muratov, 1963; studies Amidostomum spp. is reported to They occur in the air passages, trachea cause pathogenetic effects, and also noted mainly, of several coastal birds. These as a cause of death in birds (See nematodes have direct life-cycles, with McDonald, 1969). However, Nowicki et optional paratenic hosts (Barus et al, al (1995) did not find serious lesions in 1978). Bakke (1972, 1975) observed a geese infected with Amidostomum spp. high prevalence, 29.4%, of Syngamus (C.) and Epomidostomum crami Wetzel, 1931 lari in Larus canus in Norway. Nikander (n 64; prevalence 98%) . The intensity of et al (1989) reported findings of gape­ infection decreased with host age. worms (Syngamus trachea, Hovorkonema Skorping and Warelius (in press) found 20 no difference in intensity of infection bird. In certain bird specres, m some (range 1-128 specimen) in eider duck coastal regions, Contracaecum can be­ (Somateria molissima) when related to come highly prevalent. body fat. Knudsen (1965) and Porrocaecum Railliet & Henry, 1902 Christiansen (1948) studied anatids and have been reported from anatid birds in eider duck in relation to parasitation with addition to numerous land birds, and have Amidodsomum. Observation of a higher been found rarely in freshwater paratenic prevalence in female than in male eider fish hosts, the intermediate host usually duck was considered to be due to the being a soil annelid (Hartwich, 1957; different sites occupied by the two sexes Barus et al. 1978; McNeill & Anderson, (Persson at al, 197 4). It appears that in 1989; Moravec, 1971) and thus the recent studies the pathogenic effect of infection generally originate from upland Amidostomum on the bird host has been regwns. considered less marked than was the case in numerous early reports. Larvae of the genera Pseudoterranova and Dujardin, 1845, may also be Ascaridoidea: Ascaridoid parasites encountered in birds in eumarine regions. occurring in fish eating birds from coastal However, these parasites of seals and regions mainly belong to the genus whales respectively, do not establish well Contracaecum Railliet & Henry, 1912. in the bird (Olafsdottir et al, 1996). Although there are some fifty species Notes on disease: In Contracaaecum described from birds, seals and dolphins, spp. The worms are found either free, the number of valid species is apparently mainly in the lumen of the proventriculus, much lower. Hartwich (1957, 1964, 1975) or attached, in large numbers, in crater­ reported the presence only of some five like formations or ulcers, in the wall of valid species in birds from the Palaearctic the proventriculus the rest of the mucosa region. Structural studies, and studies apparently being intact (Huizinga, 1971, employing isoenzyme electrophoresis Liu & Edward ( 1971) , Greve et al ( 1986), (Cianchi et al, 1992, Paggi & Bullini, Sarashina et al ( 1987), Fagerholm et al. 1995), as well as sequencing of portions (in press). In the last cited study the host of certain genes, are in progress to (Black noddy, Anous minutus), compris­ delimitate species of this genus. By ing both adult and juvenile birds, were all analysing the distribution of caudal infected with the parasite ( Contracaecum sensory structures, in combination with magnipapillatum Chapin, 1925) with an other structural features, species, or intensity of 7 - 20 worms per host. The species groups, can be defined (Fager­ lining of the proventriculus showed local holm, 1989; 1991). inflammatory reactions to the parasites. The life cycle of Contracaecum in The muscularis interna was locally birds is similar to the one of seals obliterated, and in a young bird worms (Huizinga, 1971; Koie & Fagerholm, invaded even the muscularis externa with 1995), and include a paratenic cellular exudate invading the affected and (or) fish host. In the peritoneum or the areas. Fibrosis as well as bacterial infil­ liver parenchyme of fish the third stage tration was verified. Areas surrounding larvae attain a length of some 20-30 mm. the necrotic tissue was infiltrated by Subsequently, the adult worm may even inflammatory cells. At the host-parasite reach a length of some 80 mm usually interface frequently a hyaline cap was occmTing in the proventriculus of the formed. 21

The conclusion has been made from fish eating birds. Coastal birds are (Oglesby, 1960; Fagerholm et a! (in press) common hosts of spirurid parasites. that Contracaecum spp. in birds potenti­ Spirurids are localized in the anterior ally can contribute to host mottality. region of the gastrointestinal canal, Hoberg & Ryan (1988) considered effect predominantly in the gizzard, proventri­ on parasites, including Contracaecum, on culus or the oesophagus or in the air sacs great shearwaters, Puffinus gravis, to be and lungs but also other sites of the bird negligible in the early breeding season, hosts. because of a substantial level of body fat. The pseudolabia are very elaborate in The worms have been suggested not to some groups. Inglis (1965) analysed the feed on host tissue (Owre, 1962; morphological convergence between Huizinga, 197 1, Fagerholm et al., in parasites in the qizzard of birds of the press) but rather on gut contents and the Acuarioidea (lateral pseudolabial struc­ functional use of penetrating the mucosa tures) and (dorsal and has been suggested to fix the worms to the ventral labial structures). Bartlett (1991) favored site in the gut (Huizinga, 197 1 ). discussed the functional morphology of However, also blood feeding is suggested the cephalic structures in Acuarioidea. In to occur in ascaridoids according to that study, not the cephalic cordons, but a observations by Deardorff & Overstreet cap like structure appearing at the point of ( 1980) and Fagerholm (1988). Ulcerations attachment, named pileus, was suggested and cap formation have been recorded in to constitutes the basis for attachment. the case of numerous other ascaridoid Cordons would only serve as 'canals' for parasites, especially in seals (see Liu & liquid nutrients to reach the oral opening Edvard, 1971, McClelland, 1980, of the worm from the stomach lumen. Valtonen et al., 1989). Some specific biological and faunistic S p i r u r i d a : The Spirurida forms an information on spirurid species occurring extensive systematic entity typified by in shore and coastal birds has been worms with a bilaterally symmetrical provided by Skrjabin et al. (1965), Bakke cephalic end with more or less pro­ & Barus (1976), Barus et a! (1978). nounced pseudolabia. The oesophagus, Borgsteede & J ansen (1980). posterior to the buccal cavity, is divided Notes on disease. Pathogenetic host into a short anterior muscular section, and reactions due to spirurid infection appears a longer posterior glandular one. The to be limited. This observation conform structures of the pseudolabia, when with the experience of prof. Roy C prominent, and the buccal cavity are used Anderson, Guelph Unv. Canada as the main feature in the classification of (pers.comm.). Specific studies remain to these parasites. In the male four proximal be made. (precloacal) and six postcloacal papillae, Dracunculoidea: Dracunculidae is and a phasmid are likely to be present on represented among the bird parasites by each subventral side on the tail. As a rule two species of Avioserpens Wehr & arthropods serve as obligatory inter­ Chitwood, 1934 (A. gilliardi Chabaud & mediate hosts in practically all spirurids, Campana, 1949) and A. mosgovoyi Supry­ although some rare exceptions are known aga, 1965). They occur in hypodermal (Fagerholm & Butterworth, 1986). Larvae tissues of the hosts (Cavia spp, Podiceps of some bird spirurids may be encoun­ spp. etc.). Planktonic crustaceans serve as tered in fish tissues (Koie, 1988). Barus et intermediate hosts (Barus et al, 1978). a! (1978) reported 74 spirurid species 22

Thelazioidea: In the genus Thelazia a. Paracuaria Krishna Rao, 1951 (see (Thelaziinaea) a few, of a total of some W ong & Anderson 1982a; Anderson & thi1ty, species, are known from (eye of) Wong 1982a); coastal birds (See Batus et a! 1978). b. Cosmocephalus Molin, 1858 (see Habronematoidea: Families with Anderson & W ong 1981; W ong & numerous genera occurring as parasite in Anderson 1982b) (see also Azuma et a!, birds are: 1988); 1. Tetrameridae with a few genera c. Skrjabinoclava Sobolev, 1943 (see with bird parasites (eg. Anderson & W ong 1992; 1994; Anderson Creplin, 1846). et al., 1994; Anderson & Bratlett (in press); Wong & Anderson 1988a,b; 2. Habronematidae (mainly in 1990a,b; Wong et al., 1989); Habronematinae; some six genera with bird parasites some of which in shore­ d. Skrjabinocerca Shikhobalova, 1930 birds: Excisa Gendre, 1928; Procyrnea (see Bartlett et a!, 1989); (Chabaud, 1958); Cyrnea Seurat, 1914; e. Ancyracanthopsis Diesing, 1861 Metacyrnea (Chabaud, 1960)). Wong & (see Wong & Anderson, 1989). Anderson ( 1991) analysed the distribution Among other nematodes a few new of habronematoidean species. Seureau & species and a new genus (Voguracuaria Quentin (1983) studied the life cycle of Wong & Anderson, 1993) was recently Cyrnea sp. described in shore birds from Iceland Acuarioidea: The large number of (Wong & Anderson, 1993). Syncuaria species of the Acuarioidea live mainly Gilbert, 1927 (S. squanwta (Linstow, under the lining of the gizzard of birds. 1883) from cormorants) was analysed by This group is morphologically rather Wong & Anderson (1987), Moravec & uniform, structural differences to be found Scholz (1990), Moravec (1990), Moravec mainly in the ornamentations of the & Scholz (1994). cephalic region. Acuarioids are often Filarioidea: The Filarioidea includes divided into three subfamilies (Acuarii­ only species which produce microfilaria, nae, Seuratiinae and Schistorophinae). Of or are allied with such forms. Of the vast these Acuariinae contains a large number number of species those occurring in (15) of genera all of which have species shorebirds are included in the family occurring in coastal birds. In that group Onchoceridae. Species are reported from the number of species amounts to more the subfamilies Splendidofilariinae than 40. Especially the genera Cosmo­ (Splendidofilaria Skrjabin, 1923), Diro­ cephalus Molin, 1858 (in marine birds) filarinae (Pelecitus, Railliet & Henry, and Desportesius (Chabaud & Campana, 1910) and Lemdaninae (Lemdana Seurat, 1949) Skrjabin et al., 1965 (in Herons) 1917, Sarcone/1Ul Wehr, 1939, Eulimdana contain numerous species. (Founikoff, 1939) and Eufilaria Seurat, In numerous recent investigations, 1921). primarily by Canadian scientists the Recent studies on species of several of development, taxonomy and ecology of the these genera have been made by numerous acuarioiid species in shore Bartlett and Anderson, in particular on the birds were analyse. Genera studied genus Eulimdana (Bartlett et al. 1989; include: Bartlett 1992, 1993; Bartlett & Anderson, 1990). The studies show that the number 23

of species in this nematode genus is much Larvae of Desmidocercella numidica larger than had previously been reported. (Seurat, 1920) has been reported from the Special adaptations involving shortened vitreous body of the eye of fishes patent periods trough an early death of the (Dubinin 1949) although arthropods are adult worm (Ephemeriality), is suggested considered intermediate hosts (Skrjabin, to occur in worms to secure transmission et al. 1967; Sonin 1966, 1968; Barus et al. of offspring, contrary to solutions in the 1978). The adults are found in air sacs genus Pelecitus where worms live long and passages of fish eating birds. but produce only few microfilaria Conclusion (Reproductive Senescence) (Bartlett & Anderson 1988, 1989, Anderson & Nematodes are common parasites of Bartlett, 1994). Cohen et al. (1991) aquatic and littoral birds. Although today recently studied the life-cycle of a there are means to define by taxonomical heartworm (Sarconema) from swans. A methods the different parasite populations key to avian filarioid genera is provided there still are only few studies which by Bartlett & Anderson (1986) attempt to evaluate any impact of a parasite on the host community level. Diplotriaenoidea (a) and Aproctoidea This is partly due to factors well known in (b): Nematodes occurring in thraceal studies on other host groups including cavities or cervical subcutaneous tissue of man. E.g. Gordon and Rau (1982) needed birds have been transferred to two super­ a population of some 2000 fish to get families, a. Diplotriaenoidea, with rather some significant answers regarding large worms (females even 0.7 m parasite induced host mortality. One (Dicheilonema ciconiae (Schrank, 1788)). novel option to estimate any effects on and (b) Aproctoidea, with smaller worms. birds would be to relate parasitation to Female worms produce oviparous eggs crucial events in the life of the host bird. which as a rule reach the environment Thus there are studies which analyse the trough the digestive system. impact of parasite infections on initiation Genera found as parasites of birds, of migration, different aspects of included in these superfamilies are: breeding, and on the success of the a. Quadriplotriaena Wehr, 1935; juvenile stages. The study of Hamilton & Diplotriaena Railliet & Henry, 1909; Zuk ( 1982) evidently triggered much of Chabaudiella Diaz-Ungrfa, 1963; Mono­ this line of work. petalonema Diesing, 1861; Petrovifilaria Based on the present review it is Sonin, 1961; Dicheilonema Diesing, apparent that there are numerous parasites 1861; Hastospiculum Skrjabin, 1923; which have a detrimental impact on the Serratospiculum Skrjabin, 1915; Hetero­ birds. However, we still need to learn the spiculum Shigin, 1951; Serratospicu­ biology and life cycles of the parasites loides Sonin, 1968; before it is possible to draw conclusions b. Desmidocerca Skrjabin, 1916; concerning parasite impact. Recently Diomedenema Johnston & Mawson, Spalding & Forrester (1993 b) suggested 1952; Desmidocercella Y orke & Maple­ that a high mortality rate due to stone, 1926; Tetracheilonema Diesing, Eustrongylides infection in some bird 1861; Pseudaprocta Schikhobalova, communities, was apparently primarily 1930; Aprocta Linstow, 1883; Mawson- caused by anthropogenetic factors: local filaria Anderson & Chabaud, 1958; increased the population of Squamofilaria Schmerling, 1925. oligochaetes. This resulted in a high ---�------· 7''·'��

24

prevalence of larvae in the fish, and in the Anderson RC, W ong PL. Western Palaearctic birds. and Ethiopian species of Skrjabinoclava The present analysis points out, (Nematoda: Acuarioidea) in Icelandic although it is possible to see some kind of shorebirds (Aves: Charadriiformes) en route to set frame of the topic, the need of further breed in the New World and Greenland. Can J research on different aspects of nematode Zool l992; 70: 1861-77 parasites of marine and shore birds, and Anderson RC, Wong PL. New species of also the need of closer cooperation be­ Skrjabinoclava aculeata (Nematoda: tween researchers representing diverse Acuarioidea) from the semipalmated sandpiper fields of study. The importance of ( Calidris pusilla) (Aves: Scolopacidae ). J defining the taxonomic status of the Helminthol Soc Wash 1994; 61: 64-6 parasite populations, as a means to undestand historical and zoogeographic Anderson RC, Wong PL. The acuaroid events, is stressed. nematodes (Acuraioidea) of the upper digestive tract of new world waders and their References transmission in marine environments. Bull Scand Soc Parasitol 1996; 6: 118 Adamson ML. Phylogenetic analysis of the higher classification of the Nematoda. Can J Anderson RC, Wong, PL, Bm·tlett C.M. Skrjabinoclava aculeata Zoo! 1987; 65: 1474-82 (Acuarioidea: ) in (Calidris alpina) from Anderson RC. Nematode parasites of verte­ Both Iceland and Louisiana, USA. J brates, their development and transmission. Helminthol Soc Wash 1994; 61: 129-32 C.A.B. International, Wallingford, U.K. 1992 Azuma H, Okamoto M, Ohbayashi M, Nishine Anderson RC, Bartlett CM. Ephemerality and Y, Mukai, T. Cosmocephalus obvelatus reproductive senescence in avian filarioids. (Creplin, 1985) (Nematoda: Acuariidae) Parasitology Today 1994; I 0: 33-4 collected from the esophagus of rockhopper Eudyptes crestatus. Anderson RC, Bartlett CM. Skrjabinoclava penguin, Jpn J Vet Res inomatae Wong & Anderson, 1987 1988; 36: 73-7 (Nematoda: Acuarioidea) as a sporadic Bakke TA. Studies of the helminth fauna of parasite of the greater yellowlegs Tringa Norway XXVII: Syngamiasis in Norway. melanoleuca Gmelin (Aves : Scolopacidae). Norw J Zool 1973; 21: 299-303 Syst Parasitol ; (In press) Bakke TA. Studies of the helminth fauna of Anderson RC, Chabaud A, Willmott S, eds. Norway XXIX: The common gull, La rus CIH keys to the nematode parasites of canus L., as final host for Syngamus vertebrates. Commonwealth Agricultural (Cyatostoma) /ari (Blanchard, 1849) Bureaux 1973-1984; vols. 1-10 (Nematoda, Strongyloidea). Norw J Zoo! Anderson RC, Wong PL. Redescription of 1975; 23: 31-8 Cosmocephalus obvelatus (Creplin, 1825) Bakke TA, Barus V. Studies of the helminth (Nematoda: Acuarioidea) from Larus fauna of Norway XXXVI: The common gull, delawarensis Ord. (Laridae) (Laridae). Can J La rus canus L., as final host for Nematoda. I Zool l981; 59: 1897-1902 Qualitative and quantitative data on species of Anderson RC, Wong PL. The transmission and Ascaridoidea (Railliet & Henry, 1915). Norw J development of Paracuaria adinca (Creplin, Zoo! 1975; 23: 183-91 1846) (Nematoda, Acuarioidea) of gulls Bakke TA, Barus V. Studies of the helminth (Laridae). Can J Zool 1982; 60: 3092-104 fauna of Norway XXXVII: The common gull, 25

Larus canus L., as final host for Nematoda. II. among filarioids of shorebirds. Can J Zoo!; Qualitative and quantitative data on species of 1990; 68: 986-92 Acuariidae, Capillaridae, Strongyloididae, Bartlett CM, Anderson RC, Bush AO. Syngamidae, and Tetrameridae: with notes on Taxonomic description and comments on the host-parasite relationship. Norw J Zoo! 1976; life history of new species of Eulimdana 24: 7-31 (Nematoda: Filarioidea) with skin-inhabiting Bartlett CM. A new hypothesis concerning microfilaria in the Charadriiformes (Aves). attachment of parasitic nematodes (Spirurida: Can J Zoo! 1989; 67: 612-29 Acuarioidea) to the upper alimentary tract of birds. Can J Zool 1991; 69: 1829-33 Bartlett CM, Anderson RC Wong PL. Development of Skrjabinocerca prima Bartlett CM. New, little known and (Nematode: Acuarioidea) in Hyalella azteca unidentified species of Eulimdana (Nema­ (Amphipoda) and Recurvirostra americana toda): additional information on biologically (Aves: Charadriiformes), with comments on its unusual filarioids of charadriiform birds. Syst precocity. Can J Zoo! 1989; 67: 2883-92 Parasitol 1992; 23: 209-30 Barus V, Segejeva TP. Capillariids parasitic in Bartlett CM. Lice (Amblycera and Ischnocera) birds in the Palaearctic region, (1) Genus as vectors of Eulimdana spp. (Nematoda: Capillaria. Acta Se Nat Brno 1989; 22: 1-50 Filarioidea) in charadriiform birds and the necessity of short reproductive periods in adult Barus V, Segejeva TP. Capillariids parasitic in worms. J Parasitol 1993; 79: 85-91 birds in the Palaearctic region (2) Genera Eucoleus and Echinocoleus. Acta Se Nat Brno Bartlett CM, Anderson RC. Lemdana 1989; 23: 1-47 wernaari n.sp. and other filarioid nematodes from Bubo vtgmwnus and Asio otus Barus V, Sergejeva TP. A new genus of Tridentocapillaria (Strigiformes) in Ontario, Canada, with a capillariids from birds, gen. revision of Lemdana and a key to avian n. (Nematoda: Capillariidae). Folia Parasitol filarioid genera. Can J Zoo! 1986; 65: 1100-9 1990; 37: 67-75 Bartlett CM, Anderson RC. Some observations Barus V, Sergeeva TP, Sonin MD, Ryzhikov on Pseudomenopon pilosum (Amblycera: KM. Helminths of fish-eating birds of the Menoponidae), the louse vector of Pelecitus Palearctic Region I. Rysavy & K. M. fulicaetre (Nematoda: Filaroidea) of coats, Ryzhikov, eds. Czechoslovak Academy of Fulica americana (Aves: Grusiformes). Can J Science, Prague, 1978 Zool 1988; 67: 1328-31 Berland B. Nematodes from some Norwegian Bartlett CM, Anderson RC. Mallophagan marine fishes. Sarsia 1961; 2: I -50 vectors and the avian filarioids of Pelecitus Borgarenko LF. Helminths of birds in fu licaeatrae (Nematoda: Filarioidea) in Tadzhikistan (In Russian). Izdatelstvo Danish, sympatric North American hosts, with Dushanbe, Book 3, Nematodes, 1990 development, epizootiology, and pathogenesis of the parasite in Fulica americana (Aves). Borgsteede FHM, Jansen J. Spirurata in wild Can J Zoo! 1989; 67: 2821-33 birds in the Netherlands. In Proc. Netherlands Society for Parasitology, Spring meeting, Bartlett CM, Anderson RC. Eulimdana jloren­ 1980; 91-2 cae n.sp. (Nematoda: Filarioidea) from Micropalama himantopus (Aves: Charadrii­ Brand T, Cullinan P. Physiological Eustrongylides. formes): evidence for neonatal transmission, observations upon a larval V. ephemeral adults, and long-lived microfilaria The behavior in abnormal warmblooded hosts. Proc Helminthol Soc 1943; 10: 29-33 26

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Hartwich G. Schlauchwlirmer, Nemathel­ view of experimental infections. Parasitol Res minthes Rund- oder Fadenwi.irmer, Nematoda 1995; 81:481-9 Parasitische Rundwi.irmer von Wirbeltieren 1. Lichtenfels JR, Stroup C. Eustrongylides sp. und Ascaridida. Die Tierwelt (Nematoda: Dioctophymatoidea): First Report Deuchlands 1975; 62: 1-256 of an Invertebrate Host (Oligochaeta: Hoberg EP. Fauna] diversity among avian Tubificidae) in North America. Proc parasite assemblages: the interaction of history, Helminthol Soc Wash 1985; 52: 320-3 ecology, and biogeography in marine systems. Liu SK, Edward AG. Gastric ulcers associated Bull Scand Soc Parasitol 1996; 6: 65-89 with Contracaecum spp. (Nematoda: Hoberg EP, Ryan P. Ecology of helminth Ascaridoidea) in a Steller sea lion and a white parasitism in Puffin gravis (Procellariiformes) pelican. Wild] Dis 1971; 7: 266-7 1 on the breeding grounds at Gough Island. Can Locke LN, DeWithh JB, Menzie CM, Kerwin J Zoo] 1988; 67: 220-5 JA. A merganser die-off associated with larval Huizinga HW. Contracaeciasis in Pelicaniform Eustrongylides. Avian Disease, Ithaca 1964; 8: Birds. J Wi ld! Dis 1971; 7: 198-204 420-7 Inglis WG. The nematodes parasitic in the Madsen H. The species of Capillaria giszzard of birds: A study in morphological (Nematoda: Trichinelloidea) parasitic in the convergence. J. Helminth 1965; 39: 207-24 digestive tract of Danish gallinaceous and anatine birds with a revised list of species of Karmanova EM. Intermediate hosts of Capillaria in birds. Dan Rev Game Bioi J Eustrongylides excisus, parasite of aquatic Parasitol 1945; 1: 1-112 birds. In Russian. Tr Gel'rnintol Lab Akad Nauk SSSR 1965; 15: 86-7 McClelland G. Phocanema decipiens: Pathology in Seals. Exp Parasitol 1980; 49: Karmanova EM. Dioctophyrnidea of animals 405-19 and man and disease caused by them. In Russian. In Fundamentals of nematology. Vol. McDonald ME. Catalogue of helminths of 20. Academy of Sciences of the USSR, waterfowl (Anatidae). Special scientific report. Moscow 1968; 20: 1-262 Bureau of Sport Fisheries and Wildlife of U.S. Department of Interior, Washington D.C., Kennedy C, Lie S. The distribution and Wildlife 1996; 126: 1-692 pathogenity of larvae of Eustrongylides (Nematoda) in brown trout Salmo trutta L. in McNeill MA, Anderson RC. Development of Fernworthy Reservoir, Devon. J Fish Bioi Porrocaecum ensicaudatum (Nematoda: 1976; 8: 293-302 Ascaridoidea) in terrestrial oligochaets Can J Zoo! 1989; 68: 1447-83 Knudsen E. Arnidostorniasisand Acuariiasis in waterfowl. (In Danish). Nordisk Vet Med Measures L. Epizootiology, pathology, and 1965; 18: 38-43 description of Eustrongylides tubifex (Nema­ toda: Dioctophymatoidea) in fish. Can J Zoo! Koie M. Parasites of the European eel, 1987a; 66: 221 2-22 Anguilla anguilla (L.) from Danish freshwater, brackish and marine localities. Ophelia 1993; Measures L. The development and patho­ 29: 93-118 genesis of Eustrongylides tubifex (Nematoda: Dioctophymatoidea) in piscivorous birds. Can Koie M, Fagerholm H-P. The life-cycle of J Zool 1987b; 66: 2223-32 Contracaecum osculatum (Rudolphi, 1802) sensu stricto (Nematoda, Ascaridoidea) in 28

Measures L. The development of Eustrongy­ Nikander S, Oksanen A, Rabergh C, Sukura A, lides tubifex (Nematoda: Dioctophymatoidea) Gapeworms of birds in Finland. Information, in oligochaetes. J Parasitol 1988a; 74: 294-304 Abo Akademi, Inst. Parasitol. (Proc.XIV Symp Scand Soc Parasitol, Helsingor, Measures L. Revision of the genus Denmark) 1989; 20: 97 Eustrongylides Jagerskiold, 1909 (Nematoda: Dioctophymatoidea) of piscivorous birds. Can Oglesby LC. Heavy nematode infestation of J Zoo! 1988b; 66: 885-95 white pelican. Auk 1960; 77: 354

Michailov TK, Buniatova Kl, Nasirov AM. Okulewicz A, Koubek P. Nematode fa una of Eggs of the nematode Eustrongylides excisus some Charadriiformes from Czech Republic in true sturgeon of the Caspian Sea. (Region Brno). Wiadomosci Parazytologiczne. Parazitologiia 1992; 26: 440-2 Warszawa 1994; 40: 173-7 Moravec F. A new natural intermediate host of Olafsdottir D, Lillendahl K, Solmundsson J. the nematode Porrocaecum semitres (Zeder, Nematode infections in Icelandic seabirds. 1800). Folia Parasitol 1971; 18: 16 Bull Scand Soc Parasitol 1996; 6: 124-5 Moravec F. Proposal of a new systematic Owre OT. Nematodes in birds of the Order arrangement of nematodes of the family Pelecaniformes. Auk 1962 79: 114 Capillariidae. Folia Parasitol 1982; 29: 119-32 Paggi L, Bullini L. Molecular taxonomy in Moravec F. Revision of capillariid nematodes anisakids. Bull Scand Soc Parasitol 1994; 4: (subfamily Capillariinae) parasitic in fishes. 25-39 Studie CSAV, Praha 1987; 3: 1-116 Persson L, Borg K, Fait, H. On the occurrence Moravec F. First record of A vioserpens larvae of endoparasites in Eider ducks in Sweden. (Nematoda) from the naturally infected Viltrevy 1974; 9: 1-24 intermediate host of nematode Syncuaria Perry M. Swallowing minnows could be squamata (Linstow, 1883) from common dangerous. The Daily Herald (Gulf Publishing cormorants (Phalacrocorax carbo (L.)) in Company) June; 1982 Czechoslovakia. Folia Parasitol 1990; 37: 93-4 Roffe TJ. Eustrongylides sp. epizootic in Moravec F, Prokopic J, Shlikas A. The young common egrets (Casmerodius albus). biology of nematodes of the family Avian Dis 1988; 32:143-7 Capillariidae Neveu-Lemaire, 1936. Folia Parasitol 1987; 34: 39-56 Sarashina T, Tanyiyjama H, Yamada J. A case of Contracaecum sp iculigerum (Ascaridoidea: Moravec F, Scholz T. First record of the Anisakinae) infection in a cormorant nematode Syncuaria squamata (Linstow, (Phalacrocorax carbo). Nippon Juigaku 1883) from common cormorants (Phala­ Zasshi 1987; 49: 15-21 crocorax carbo (L.)) in Czechoslovakia. Folia Parasitol 1990; 37: 365-6 Seureau C, Quentin JC. Larval biology of Cyrnea (Cyrnea) eurycerca Seurat, 1914, a Moravec F, Scholz T. Observations on the habronematidid nematode parasite of the development of Syncuaria squamata (Nema­ francolin in Togo.(In French). Ann Parasitol toda: Acuariidae), a parasite of cormorants, in Hum Camp 1983; 58: 151-64 the intermediate and paratenic hosts. Folia Parasitol 1994; 41: 183-92 Shirazian C, Schiller EL, Glaser CA, Vonderfecht SL. Pathology of larval Nowicki A, Roby DD, Woolf A. Gizzard Eustrongylides in the rabbit. J Parasitol 1984; nematodes of Canada geese wintering in 70: 803-6 southern Illinois. J Wild! Dis 1995; 31: 307-13 29

Simpson VR, Harris EA. Cyathostoma lari Sprinkle DJ. Life history studies of (Nematoda) infection in bird of pray. Proc Eustrongylides tubifex (Nitzsch, 1918) Zoo! Soc London, J Zoo! 1992; 227: 655-9 Higerskii.ild, 1909 (Nematoda: Diocto- phymatida) M.Sc. thesis, Ohio State Skirnisson K, Jonsson AA. Parasites and University, Columbus, 1973 ecology of the common eider in Iceland 1996; Bull Scand Soc Parasitol 1996; 6: 126-7 Sprinkle-Fastzkie J, Crites J. A redescription of Eustrongylides tubifex (Nitzsch, 1819) Skorping A, Warelius K. (In press) Parasitism Jagerskii.ild, 1909 (Nematoda: Dioctophyma­ and host reproductive success: early laying tidae) from mallards (Anas platyrhynchos) J eiders have higher lipid stores, more parasites Parasitol 1977; 63: 707-12 and better parasite tolerance Valtonen ET, Fagerholm HP, Helle E. Sktjabin KI, Sobolev AA, Ivaschkin VM. Contracaecum osculatum (Nematoda: Osnovi nematodologii (In Russian) Vol 14. Anisakidae) in fish and seals in Bothnian Bay Spirurata. Part Ill. Acuarioidea. Moscow: (Northeastern Baltic Sea). Intern J Parasit Izdat. Nauka 1965 1988; 18: 365-70 Sonin MD. Filariata of animals and man and Watters C.E. Cyathostoma infection as the the diseases caused by them. Part I. cause of respiratory distress in emus Aproctoidea (In Russian). In Skrjabin, KI, ed. (Dromaius novaehollandiae). In: Kornelsen, Principles of Nematodology. Moscow, M. J. (Ed.) Proc. Ass. Avian Veterinarians, Izdatelsvo "Nauka" 1966; Vol 17: 1-360 Revo, Nevada, USA 1994; 151-5 Sonin MD. Filariata of animals and man and Wiese JH, Davidson WR, Nettles VF. Large the diseases caused by them. Part 2. scale mortality of nestling ardeids caused by Diplotriaenoidea (In Russian). In Skrjabin KI, nematode infection. J. Wild!. Dis. 1977; 13: ed. Principles of Nematodology, Moscow, 376-82 Izdatelsvo "Nauka"; 1968: Vol 21: 1-388 Wong PL, Anderson RC. Redescription of Soulsby EJL. Helminths, arthropods and Paracuaria adunca (Creplin, 1846) protozoa of domesticated animals, 7th edition. (nematoda: Acuarioidea) from Larus London: Bailliere Tindall; 1986 delawarensis Ord. (Laridae) Can. J. Zoo!. Soveri T, Oksanen A, Sukura A, Nikander S, 1982a; 60: 175-9 Jalanka H. Annually occuning parasitic W ong PL, Anderson RC. The transmission tracheobronchitis in the barnacle goose and development of Cosmocephalus obvelatus (Branta leucopsis) at the Helsinki zoo. (Nematoda: Acuarioidea) of gulls (Laridae). A Information, bo Akademi, Inst. Parasitol. Canadian Journal of Zoology 1982b; 60: (Proc XIV Symp Scand Soc Parasitol, 1426-40 Helsingi.ir,Denmark) 1989; 20: 73 Wong PL, Andersson RC. Development of Spalding MG, Forrester DJ. Pathogenesis of Syn cuaria squamata (Linstow, 1883) Eustrongylides ignotus (Nematoda: Diocto­ (Nematoda: Acuarioidea) in ostracods (Ostra­ phymatoidea) in Ciconiiformes. J Wild! Dis coda) and doublecrested cormorants (Phala­ 1993a; 29: 250-60 crocorax auritus auritus). Can J Zoo! 1987; Spalding MG, Forrester DJ. Epizootiology of 65: 2524-3 1 in wading birds (Ciconii­ Wong PL, Anderson RC. Skrjabinoclava formes) in Florida. J Wild! Dis 1993b; 29: bartlettae n.sp. (Nematoda: Acuarioidea) from 237-49 the black-bellied plover (Pluvialis squatarola 30

(L.)) (Charadriiformes: Charadriidae). Can J Zieris H, Betke P. Cyathostoma bronchialis Zoo! 1988a; 66: 2262-4 (Muhling, 1884) Ordnung Strongylida, Familie Syngamidae bei Mandarinenten (Aix W ong PL, Anderson RC. Transmission of galericulata) als Todeursache. Monatshefte fur Skrjabinoclava morrisoni Wong and Veterini:irmedizin 1991; 46: 146-9 Anderson, 1988 (Nematoda: Acuarioidea) to semipal mated sandpipers ( Calidris pusilla (L.)) (Charadriiformes: Scolopacidae). Can J Zoo! !988b; 66: 2265-9 Wong PL, Anderson RC. Ancyracanthopsis winegardi n. sp. (Nematoda: Acuarioidea) from Pluvialis squatarola (Aves: Charadrii­ dae) and Ancyracantus heardi n. sp. from Rallus longirostris (Aves: Rallidae), and a review of the genus. Can J Zoo! 1989; 68: 1297-306 Wong PL, Anderson RC. Host and geographical distribution of Skrjabinoclava spp. (Nematoda: Acuarioidea) in Nearctic shorebirds (Aves: Charadriiformes) and evi­ dence for transmission in marine habitats in staging and wintering areas Can J Zoo! 1990; 68: 2539-52 Wong PL, Anderson RC. Distribution of qizzard nematodes (Habronematoidea, Acuari­ oidea) of New World shorebirds (Charadrii­ formes), with special reference to localities of transmission. Can J Zoo! !991; 69: 2579-88 Wong PL, Anderson RC. New and described species of nematodes from shorebirds (Charadriformes) collected in spring in Iceland. Syst Parasitol 1993; 25: 187-202 Wong PL, Anderson RC, Bartlett CM. Development of Skrjabinoclava inornatae (Nematoda: Acuarioidea) in fiddler crabs (Uca spp.) (Crustacea) and Western (Catoptrophorus semipalmatus inornatus) (Aves: Scolopacidae). Can J Zoo! 1989; 67: 2892-901 Wong PL, Bartlett CM, Measures LN, McNeill MA, Anderson RC. Synopsis of the parasites of vertebrates of Canada, Nematodes of Birds. Alberta Animal Health Division, Alberta; 1990 Bull Scand Soc Parasitol 1996; 6 (2): 31-49

LIFE CYCLES AND DISTRIBUTION OF SEABIRD HELMINTHS IN ARCTIC AND SUB-ARCTIC REGIONS

K.V. Galaktionov Murmansk Marine Biological Institute, Murmansk, Russia1

Seabird helminths have complicated From this point of view, I will at­ life cycles with frequently more than one tempt to analyse some special futures of intermediate host involved. In addition seabird helminth distribution in the nor­ the inclusion of free-living stages in the thern regions (the Barents, White, Nor­ life cycles ensures the dispersal of the wegian and Greenland Seas, mainly). parasites. The successful completion of Most attention will be paid to tremato­ the life cycles depends on the favourable des, cestodes and acanthocephalans. combination of many factors in both the Nematodes will be considered by Dr. macro- and microenvironment. Consequ­ Fagerholm (this volume). ently, an analysis of the seabird parasite 1. Helminth life cycles and specific fauna in any geographical area must take features of the helminth fauna in into account all the stages of each para­ different groups of marine and coastal sites life cycle and the biology of the birds host species involved. Such a approach was used in V .A.Dogel's (1941) classical The trematode basic life cycle invol­ studies on ecological parasitology, and ves two intermediate hosts. Gastropod later developed by many investigators molluscs (bivalves for Gymnophallides, (James, 1968a; Kennedy, 1975; Ginet­ only) act as the first one, and different zinskaya & Dobrovolskii, 1983; Holmes, invertebrates and fishes as the second. 1986; Bush, 1990; Combes, 1991; etc.). This life cycle may include two free­ We must emphasise that the parasites swimming larval stages: miracidiae and found in a particular host (seabirds) cercariae. However, in many trematodes cannot be viewed in isolation. There are miracidia do not hatch from the eggs, many stages in the life cycle of each and the first intermediate host becomes parasite and all are equally important for infected by ingesting the eggs containing its completion and success. As a result developed larvae. The second interme­ any environmental factors which influ­ diate host may be omitted from the life ence the fitness of any of the hosts will cycle which is typical of microphallids effect the well-being of the parasites. of the "pygmaeus " group which are

1 Current address: Zoological Institute, St Petersburg, Russia 32 distributed widely over northern regions. life cycles are similar to those described In this case, metacercariae mature inside for cyclophyllides. Mature females para­ the sporocysts parasitizing the molluscan sitizing birds disperse eggs. Together host which combine, to some extent, the with pellets they enter the water and sink functions of both the first and second to the bottom where they may be inge­ intermediate hosts. Life cycles devoid of sted by benthic crustaceans (intermediate larval stages which are free in the envi­ hosts for acanthocephalans). Cystacanths ronment (miracidia and cercariae, in case (invasive larvae for the definite host) of trematodes), are called "autonomic". develop within them. In some species, This name reflects the fact that they are transport (paratenic) hosts - fishes - less dependant on environmental factors become peripherally involved in the life (James, 1968a; Galaktionov; 1987; 1993; cycles. Galaktionov, 1996; Bustnes, 1996). Even a cursory examination of the Of the cestodes, specimens from two life cycles of the helminth groups in orders (Tetrabothriidea and Cyclophylli­ question permits us to conclude that dea; fams. Dilepididae and Hymenolepi­ completion of most life cycles is only didae) are associated with seabirds. possible in coastal ecosystems. For Tetrabothriid life cycles usually involve trematodes, the limiting factor is the two intermediate hosts (Temirova & obligatory participation of molluscs (i.e. Skryabin; 1974; Hoberg; 1987; 1989; benthic animals) in the life cycle. Ben­ 1991). The first is represented by plank­ thic crustaceans are intermediate hosts tonic crustaceans, the larva - procercoid - for acanthocephalans, hymenolepidid is formed inside them. The crustaceans and some dilepidid cestodes. Dispersion are infected by ingesting on parasite eggs efficiency in some trematodes and a­ distributed with seabird pellets. Further canthocephalans increases to some development of the parasite takes place extent due to the incorporation of fishes after ingestion of infected crustaceans by as second intermediate and paratenic cephalopods or fishes. Inside them the hosts, respectively. However, with few infective larva - plerocercoid - is formed. exceptions, the fish involved do not Due to the fact that Tetrabothriidea include pelagic species - the main forage plerocercoids are morphologically very for seabirds. For example, the interme­ similar to those of Pseudophillidea and diate hosts of Corynosoma spp. (a wi­ Tetraphyllidea, there would appear to dely-distributed acanthocephalan of have been some misidentification of marine mammals and birds) are bottom these organisms in the past. Until the dwelling amphipods, Pontoporeia and study by Hoberg (1987), all uniacetabu­ Gammarus (Petrochenko, 1958; Khok­ late plerocercoids recorded in fishes hlova; 1986; McDonald; 1988). Numer­ were ascribed to the Pseudophillidea and ous species of benthophagous fishes are Tetraphy llidea. recorded as the paratenic hosts and this Dilepididae and Hymenolepididae also restricts the parasite transmission to have the same general pattern involving the coastal zone (Hoberg, 1985; our one intermediate host which is, as a rule, data). a crustacean. Unlike tetrabothriides, A different situation arises in tetra­ gravid proglottids or parts of strobile bothriides, which evolution is closely rather than individual eggs, are emitted connected with pelagic ecosystems into the environment. Acanthocephalan (Temirova & Skryabin; 1974; Hoberg, 33

1987; 1989). Use of pelagic invertebrates birds as the final hosts. In the deeper and and fishes as intermediate hosts permits more off-shore regions, molluscs are them to successfully complete their life mainly infected by parthenites and larvae cycles in the open sea. This is also true of fish trematodes (Chubrik, 1966; K0ie, for some dilepidides (for example, A/ea­ 1983; 1984; Galaktionov & Marasaev, taenia farina and A. armillaris) which 1990). cysticercoids were recorded in plankto­ Under certain conditions, foci of nic euphausiid crustaceans (Shimazu, seabird infection with helminths may be 1975). formed well off-shore. We observed this In the coastal zone the successful in the south-eastern part of the Barents completion of the life cycles is also Sea (also referred to as the Pechora Sea) promoted by a relatively high (as compa­ (Fig. 1 ). Here the prevalence of sub litto­ red to the open sea) density and diversity ral molluscs ( i.e. Margarites groenlan­ of birds. The littoral-upper sublittoral dicus, Solariella varicosa and Crypto­ regions are of special importance as the nautica clausa) with parthenites and life cycles of most trematodes, acantho­ larvae of the "pygmaeus " group microp­ cephalans and many cestodes (the adults hallids, reached 50 to 70% (Galaktionov of which parasitize seabirds) are mainly & Marasaev, 1986). Previously, such connected with this zone. It is in these high prevalences had only been recorded regions that contact between interme­ in tidal zones. The significance of the diate (bottom invertebrates) and final Pechora Sea region is that the greatest (coastal and marine birds) helminth hosts values (for the Barents Sea) of biomass occurs. As a result, larval stages of of benthic invertebrates (including seabird helminths constitute a predomi­ molluscs) have been recorded there. At a nant component of the infection of depth of ea. 20-25 m they become avai­ coastal invertebrates. So, of 21 species lable for marine ducks, especially eiders. of trematode parthenites and larvae Flocks consisting of many thousands of recorded in the Barents Sea littoral eiders accumulate there during their molluscs, 16 in their adult stage parasiti­ autumn migrations from the east. During ze birds (Chubrik, 1966; Podlipaev, brief stop-over, the birds feed on the 1979; Galaktionov & Marasaev, 1990; molluscs, become infected and subsequ­ Galaktionov & Bustnes, 1996). Studies ently disperse the invasional agent elsewhere have demonstrated similar (eggs). This is promoted by the rapid numbers of parthenites and larvae: 20 development of the adult flukes (3 or 4 and 16 for Littorina spp. (James, 1968b); days). 16 and 12 for Hydrobia ulvae (Saville, Taking into account that most parasi­ 1992) on British Isles coast; 11 and 10 tic helminths of coastal and marine birds for L. saxatilis (Combescot-Lang, 1976); use invertebrates as intermediate hosts, it and 46 and 30 for Hydrobia spp. could be suggested that the highest (Deblock, 1980) on the French coast; 6 parasite species diversity is likely to be and 5 for L. littorea on the North Sea recorded in those birds having a diet coast (Werding, 1969), etc. As a result of which consists mainly of invertebrates. a long-term investigation at the north­ In fact, the most diverse (both quantitati­ eastern coast of the U.S.A., Stunkard vely and qualitatively) parasite fauna is (1983) revealed parthenites and larvae of recorded in the benthophagous common 4 7 trematodes in the littoral - upper eider. The high variability of their diet in sublittoral molluscs; 21 of them used different parts of the distribution area 34

° 70

68°

Fig. 1. Distribution of the prevalence of subtidal molluscs (Margarites groenlandicus, Solariella varicosa and Cryptonautica clausa) with parthenites and larvae of the "pygmaeus " group microphallids in the south-eastern part of the Barents Sea (the Pechora Sea) • Prevalence: 11-up to 5%; -5-10%;

- 10-20%; - 20-30%; - more than 30%

(Madsen, 1954; Bagge et al, 1973; gull) possess an abundance and diversity Cantin et al, 1974; Bianki et al, 1979; of helminths which are slightly greater Bustnes & Erikstad, 1983; etc.) results in than those of eiders and waders. So, in the fact that also the helminth species herring gulls, 13 trematode and cestode composition varies considerable in species were recorded in Britain and different regions (Belopolskaya, 1952; Northern Ireland (Pemberton, 1963; Kulatchkova, 1958; Lapage, 1961; Threlfall, 1967; Irwin & Prentice, 1976), Person et al, 1974; Grytner-Ziecina & 18 species at the North Sea coast (Loos­ Sulgostowska, 1978; Galaktionov et al, Frank, 1971), 12 species at Newfound­ 1993; etc.). land (Threlfall, 1968), and 16 species at An extremely rich trematode and the East Murman (Belopolskaya, 1952). cestode fauna has been recorded in The greatest number of parasites - 16 waders feeding on littoral invertebrates trematode species and 11 cestode species (Belopolskaya, 1959; Bykhovskaya­ was recorded in common gulls in the Pavlovskaya, 1962; Bush, 1990; etc.). west coast of Norway (Bakke, 1972a; With rare exceptions, these birds are 1972b; 1985), but not all of those para­ only associated with the sea coasts sites completed their life cycles in coas­ during winter and are not included in the tal-water ecosystems. In kittiwake, a seabird group. Gulls (especially such more specialized fish-eater, a smaller euriyphagous species as the common number of helminthes was recorded: 4 gull, herring gull and great black-backed trematodes and 4 cestodes at the East 35

Murman coast (Belopolskaya, 1952). invertebrates in which the ability to This trend was more pronounced in migrate is less than in the vertebrates guillemots. Trematodes had almost associated with the life cycles concerned disappeared from their parasite fauna, (Ginetzinskaya & Shtein, 1961; Ginet­ and cestodes were mainly represented zinskaya, 1983; 1988). The spotted with species from genus Alcataenia and distribution pattern of infection with Tetrabothrius (Belopolskaya, 1952; helminth larvae is even observed in Bear, 1956; 1962; Threlfall, 1971; oceanic plankton. Moreover, it has been Hoberg, 1986). The poorest helminth shown that the highest concentrations of fauna is typical for planktonphagous infected specimens occur in zones of species. Of the 48 little auks sampled in circulation and upwelling (Kurochkin, the North Atlantic region, 6 birds contai­ 1976; Kurochkin & Pozdnyakov, 1980). ned 2 specimens of Tetrabothrius sp. and We will attempt to use these ideas for 4 specimens presumably Alcataenia sp. the analysis of specific features of the (Threlfall, 1971). Of the 15 little auks distribution of the seabird trematode dissected by us at the J osef Land, patihenites and larvae throughout littoral only one contained an immature speci­ molluscs in the Barents, White and men of Alcataenia sp. Norwegian Seas (Galaktionov & Bust­ nes, 1996). This study involved compu­ 2. Life cycles and distribution pattern terized data from the parasitological of seabird trematodes along the coasts observation of 35 000 periwinkles of the Northern European seas (Littorina spp.). The molluscs were It is well known that parasite fauna collected from 180 stations at the No­ composition in animals, including sea­ vaya Zemlya and Vaigach Island coasts birds, differs from region to region. It is (Region A), White Sea (Region B), determined by how the conditions in any Eastern Kola coast (Region C), Western region favour completion of the life Murman and Eastern Finmark (Region cycle of each helminth species. Firstly, it D), Western Finmark and Tromsp depends on specific features of the life (Region C) (Fig. 2). The region A is cycle itself: presence or absence of free­ characterised by its severe Arctic clima­ living stages, larval biology, reproducti­ te, conditions become progressively ve pattern of the adults, and so on. The milder to the west. probability of completion is determined We found the parthenithes and larvae by the combination of the two complex of 14 trematode species. Marine birds factors: 1) environmental conditions and are the final hosts of 13 of them. The 2) specific features of the biology and exception was Podocotyle atomon which ecology of the intermediate and final uses fish as a definitive host. Among the hosts. final hosts, the most important marine These factors are subject to large­ birds are the common eider and the large scale and small-scale variables as illus­ gulls (herring gull, great black-backed trated by geographical scales of measu­ gull and common gull). rement on one hand, and habitat (or even For analysis we divided the tremato­ microhabitat) scale on the other. The des into 4 groups: latter determines uneven distribution of parasites over the host population in any Group I - Microphallids of the region. Very often foci of high infection "pygmaeus" group. The 4 closely related occur. This is especially pronounced in species of genus (M. 36

Fig. 2. Map of the Barents, White and Norwegian Seas coast showing the regions studied in 1978-1 994 (after Galaktionov & Bustnes, 1996) Region A-the Novaya Zemlya and Vaigach Island coasts; Region B-the White Sea; Region C - Eastern Kola coast; Region D - Western Murman and Eastern Finmark ; Region E-Western Finmark and Troms0. pygmaeus, M. piriformes, M. pseudo­ We found a significant increase in the pygmaeus, M. triangulatus) with auto­ number of trematode species at the nomic life cycle. sampling locations in the direction from Group II - common seabird (mainly east to west (Table I). The main diffe­ gull) trematodes with free-living stages rence in the composition of trematode in their three-host life cycles. Himasthla fauna in both L. saxatilis and L. obtusata sp. has both free-swimming miracidia between regions was the number of and cercariae, Microphallus similis, species with free-living larval stages (1 Cryptocotyle lingua and Renicola sp. or 2) in their three-host life cycles (Table only cercariae. I). The number of these species was highest in the western regions. In the Group Ill - rare seabird trematodes easternmost region A, only Notocotylus (Maritrema arenaria, M. murmanica, sp. and Podocotyle atomon, were found. Parapronocephalwn symmetricum, Microphallids of the "pygmaeus" group, Notocotylus sp., Parvatrema sp.). with autonomic life cycles were found Group IV - Podocotyle atomon by everywhere. itself. This trend is shown clearly by calcu­ lating the frequency of occurrence 37

Table 1. Occurrence of trematode parthenites and larvae in intertidal molluscs in the different regions (A-E) of the Barents, White and Norwegian Seas (after Galaktionov & Bustnes, 1996)

Trematode species First intermediate host Littorina obtusata A B c D E A B c D E

Microphallus pygmaeus + + + + + 0 + + + + M. piriformes + + + + + 0 + + + + M. pseudopygmaeus + + + + + 0 + + + + M. triangulatus + + + + + 0 + + + + M. similis + + + + 0 + + + + M aritrema arenaria + + 0 + + M. murmanica + 0 Cryptocotyle lingua + + + + 0 + + + Renicola sp. + + + + 0 + + + Himasthla sp. + + + + 0 + + Parvatrema sp. + + + + 0 + + + Notocotylus sp. + + + + + 0 + + Parapronocephalum sym- + + + 0 + + + metricum Podocotyle atomon + + + + + 0 + + + + 0-absence of molluscs in region; - absence of trematode species in mollusc; + presence of trematode species in mollusc

(Galaktionov & Bustnes, 1996), which is longitudinal changes in environmental the percentage of each trematode species condition, which are more favourable in (group of species) among the infected western regions. This fact facilitates the snails in the region. In all regions, micro­ completion of trematode life cycles phallids of the "pygmaeus" group (Group which include several hosts and free­ I) occupied a central place (Fig. 3). living stages. This is probably the reason Frequency of occurrence of these para­ why there was an increase in frequency sites had a maximal value in regions B of occurrence of trematodes with these and C, then decreased in the western life cycles (Group II and Group III) in regions D and E. On the other hand, the both L. saxatilis and L. obtusata in west­ frequency of Group II trematodes inCI·ea­ ern direction (Fig. 3). Only one excepti­ sed steadily in the western direction in L. on from this rule was found, P. atomon, saxatilis from 0% in region A to about probably caused by some specific traits 45% in region E, and in L. obtusata from in its life cycle. 5% in region B to about 25% in region The general decrease in frequency of E. The trends were less pronounced for occurrence of trematodes with autono­ the other parasites, which were only mic life cycles (Group I) in the western found at a low frequency. regions (D and E) may partly be deter­ The interregional differences in mined by the increase of competition frequency of occurence of trematode from the species from Groups II and Ill. species are determined largely by the 38

conditions. In addition to microphallids c::::J Group 1 100 - Llttorlna saxatllls f'Z?im Group 2 of the "pygmaeus" group, they are typi­ f::;-':ill Group 3 cal for the "terrestrial" trematodes in the ��:;:� P .atomon 80 families Brachylaemidae and Dicrocoe­

60 Iiidae. Under more favourable conditions for existence, advantages of trixenic life 40 cycles become obvious. As a result, 20 - "pygmaeus" microphallids, which pre­ dominate in the Barents Sea and the

A B c 0 E White Sea molluscs, surrender their

REGION dominance towards the west (towards region E). Continuation of this trend results in an absolute domination by

C-=:J Group 1 trixenic trematodes in periwinkle infec­ Llttorlna obtusata G"S3 Group 2 tion on the seashores of Germany, Fran­ 100 t:R:."l..� Group3 oora p. atomon ce, Britain and Northern Ireland 80 (Werding, I 969; Lauckner, I 980; Com­

60 bescot-Lang, 1976; James, I 969; Hughes & Answer, I 982; Irwin, I 983; Matthews 40 et al, I 985; etc.). Longitudinal changes in host distri­ bution also greatly influence the pattern B c 0 E of trematode distribution in the regions REGION under consideration. The relatively low prevalence of the gull trematodes M. Fig 3. Frequency of occurrence of tre­ similis and C. lingua in the regions B matode groups (I-IV) in the intertidal and C, may be connected with that periwinkles Littorina saxatilis and L. phenomenon. obtusata in regions (A-E) (after Galakti­ The second intermediate host of M. onov & Bustnes, 1996) (explanations in similis is the seashore crab, Carcinus the text) maenas, which is absent east of the The transference to dixenic cycles Varanger Fj ord. Metacercariae of this results in some negative consequences: trematode can also develop in the subti­ the range of the final hosts becomes dal crab Hyas araneus (Uspenskaya, narrower, dispersion by the second I 963; Podlipayev, I 979), but it is rarely intermediate host in the environment found in the intertidal zone and therefore disappears, the additional supply of cannot serve as an agent of intensive energy at the expense of its second infection for M. similis. This example intermediate host is absent, and so on highlights another advantage of dixenic (Galaktionov, 1987; 1993). Clearly, life cycles in the Arctic and sub-Arctic trixenic life cycles with 1 or 2 free-living regions where there is restricted diver­ larvae are distributed most widely among sity of potential intermediate hosts. trematodes. We consider that secondary The situation is different for C. origin of a dixenic autonomous life cycle lingua, because the fishes associated is an adaptation for completion in ecosy­ with the intertidal zone (second interme­ stems with extreme environmental diate hosts) are also numerous in eastern 39

regions. A possible explanation for the low prevalence of this parasite in peri­ winkles in the eastern regions is that the main first intermediate host L. littorea is very rare in those areas. The other po­

tential hosts - L. saxatilis and L. obtusata are not able to support an intensive circulation of C. lingua under the relati­ vely harsh environmental conditions of the eastern seashore. So far I have dealt with the macro­ scale, i.e. inter-regional differences. But the same factors determine the micro­ scale distribution of infection of the molluscs studied. The example of echi­ nostomatid Himasthla sp. is very ob­ vious. Both intermediate hosts (peri­ winkles and blue mussels) and final hosts (gulls) are common on the Barents Sea coast. However, the presence of free-swimming miracidia and cercaria in the life cycle prevents distribution of this Fig. 4. Distribution of prevalence (%) of species to the east (see above). On the Himasthla sp. in periwinkles Littorina exposed seashores of the Kola coast, no saxatilis along the coast of Y arnishnaya infection of periwinkles was observed, Bay (Eastern Murman) whereas in the bays protected from wave action, local foci of Himasthla sp. infec­ 3. Life cycles and latitudinal distribu­ tion were found. In the most sheltered tion of seabird helminthes regions (termination) of Yarnyshnaya Unfortunately, at present we have Bay investigated by us (Fig. 4), preva­ little substantiated information on the lence of rediae in periwinkles reached distribution of seabird cestodes and 7.3% and prevalence of metacercariae in acanthocephalans in the Arctic and sub­ blue mussels was 100% with an intensity Arctic ecosystems. In our opinion, up to 200 specimens. One hundred per however, the theories concerning factors cent of the herring gulls were infected limiting life cycles to particular ecologi­ with adult Himasthla sp. in Y arnyshnaya cal conditions in trematodes, may also Bay and the parasite load reached 1000 apply to other helminths. On this basis, specimens per bird (Galaktionov et al, in let's analyse the seabird helminth fauna prep.). At the same time, no infection of in the northern regions. gulls with Himasthla sp. was revealed in a region just 30 miles away from Yarnis­ In the high Arctic at Franz J osef hnaya Bay - at Seven Islands archipelago Land archipelago, we carried out para­ (Galaktionov, 1995). sitological studies in 1990-93 (Galak­ tionov & Marasaev, 1992; Galaktionov 40

Table 2. Composition of the helminth fauna of the Franz Josef Land in marine and coastal birds in 1991-1993

Bird species Number of Cestoda Acanthocephala dissected Prevalence Range in Prevalence Range in birds % intensit� % intensity

Kittiwake ad. 17 82.3 1-52 1 1.8 2-4 ( R issa tridactyla) JUV. 4 100 1-8 0 ()

Glaucous gull ad. 8 75.0 2-11 0 0 (Larus hyperboreus) JUV. 4 100 1-10 0 0

Arctic tern ad. 11 9.1 72.7 8-227 (Sternaparadisa ea)

Brunnich's guillemot ad. 13 46. 1 1-10 () 0 (Uria lomvia) JUV. 5 100 2-26 0 0

Black guillemot ad. 11 27.3 1-7 I 8.2 (Cepphus grylle)

Little auk ad. 15 6.7 0 0 (Alle alle)

Purple sandpiper ad. 7 28.6 3- 142 14.3 2 (Calidris maritima)

et al, 1993; Galkin et al, 1994). First of (Table 3). The molluscs Margarites heli­ all, a complete absence of trematodes cinus and M. groenlandicus umbilicalis from the parasite fauna of the archipela­ act as the first intermediate hosts. go gulls and guillemots seems to be Life cycles of cestodes and a­ significant (Table 2). The severe Arctic canthocephalans, which as adults parasi­ climate acts as a limiting factor and in tize seabirds, are better adapted for the the coastal zone inhibit transmission of completion in the Arctic coastal ecosy­ life cycles with free-swimming larvae. stems. It should be emphasised, that they Moreover, many boreal and arctic-boreal are devoid of free-swimming larvae, i.e. molluscs (Littorina spp., Onoba aculeus, they are completely autonomic and, with Hydrobia ulvae, etc.) which are first the exception of Tetrabothriidea, involve intermediate hosts for trematodes, do not only two hosts. The successful transmis­ occur in the High Arctic. The only sion of these parasites is also enhanced trematode species recorded by us in the by the abundance of crustaceans (ben­ Franz Josef Land region (Microphallus thic, planktonic and connected with pseudopygmaeus) belongs to the "pyg­ cryopelagic communities) in the Arctic maeus" group and has a completely auto­ coastal zone. All of them are eaten by nomic life cycle. The adults are recorded birds and they form the main items of in the common eider in which the worm the common eider diet (Weslawski et load reaches several thousand specimens 41

Table 3. Infestation of the common eider (Somateria mollissima) by the most com­ mon helminths in the different parts of the northern seas

Helminths Age Franz Josef Seven Island Kandalaksha group of Land* archipelago** Gulf of the birds (Eastern White Sea*** Muman )

PREY INT PREY INT PREY INT

% % % Microphallids of the ad. 55.6 1000 76.0 24000 lOO 36000 "pygmaeus" group juv. 80.0 35000 91.7 9500 100 640000 CESTODA Microsomacanthus spp. ad. 100 240000 60.0 19500 100 20000

juv. lOO 155000 40.0 10000 100 55000 ACANTHOCEPHALA Polymorphus phippsi ad. 100 !007 4.0 75.0 16 juv. 100 937 75.0 247 64.3 57 *-our data; ** - after Beloplskaya, 1952; *** - after Kulatchkova, 1979 PREY - prevalence, %; INT - maximal intensity of infestation al, 1994). In the more southern regions of thus spp. and the acanthocephalan Poly­ the Barents Sea common eiders feed morphus phippsi. The infection greatly mainly on molluscs (Bianki et al, 1979; exceeds that in the seabirds at the Mm­ Shklyarevich & Shklyarevich, 1982). man coast of the Barents Sea and the White Sea (Table 3). For the same Thus, the high levels of infestation reason, 80% of the Arctic terns were with cestodes which were recorded in heavily infected with acantocephalan P. the Franz Josef Land birds (Table 4), are phippsi (an unusual parasite for the� in not surprising. Consumption of plankto­ other regions) which is unable to achieve nic crustaceans results in the infestation maturity in them. of guillemots with Alcataenia armilla is, � Transmission of tetrabothriids near and kittiwakes and glaucous gulls, with the archipelago is probably connected A. farina. Feeding on coastal amphipods with Arctic cod (Boreogadus saida) may be reflected in the infection of the which constitute the bulk of the diet of latter two birds with A.micracantha and fish-eating birds. In kittiwakes feeding Microsomacanthus ductilis. Prevalence mainly on Arctic cod in August, 1991, and intensity of infection by these cesto­ we revealed T. erostris which had attai­ des in kittiwakes exceed the values ned the developmental stages which recorded at the southern coast of the follow the uniacetabulate plerocercoid Barents Sea. The above-mentioned (Galkin, in prep.). Probably, tetrabothriid increase in the proportion of gammarids larvae are contained in the metacestode in the common eider diet by the archi­ complex identified in many of the Ea­ pelago results in the high infestation rents Sea fishes as Scolex pleuronectis with the hymenolepidid Microsomacan- (Poljanskiy, 1955; Zubchenko & Kara- 42

Table 4. Composition of the cestode fauna of seabirds of Franz Josef Land and Seven Island archipelago (Eastern Murman) in 1991-1993

Cestode species Franz Josef Land Seven Island Prevalence Maximal Prevalence Maximal % intensity % intensity

KITTIWAKE (Rissa tridactyla) Alcataenia farina 28.6 2 69.0 120 A. armillaris 0 0 3.4 5 Anomotaenia micracantha 28.6 5 0 0 Microsomacanthus ductilus 14.3 10 0 0 Nadejdolepis nutidulans 0 0 3.4 Tetrabothrius erostris 71.4 16 31.0 4 T. immerinus 0 0 3.4 1 T. morschtini 7.1 0 0 GLAUCOUS GULL (Larus hyperboreus) Anomotaenia micracantha 12.5 1 Microsomacanthus ductilus 25.0 6 Te trabothrius erostris 87.5 10 T. morschtini 25.0 2 BRUNNICH'S GUILLEMOT (Uria lomvia) Alcataenia armillaris 53.8 6 20.0 2 Microsomacanthus ducti/us 16.7 7 0 0 Te trabothrius sp. 16.7 12 0 0 BLACK GUILLEMOT (Cepphus grylle) Alcataenia campylacantha 27.3 11 40.0 11 sev, 1986). High infestation with these our data) are recorded. Their life cycles larvae is also described in Arctic cod are associated with the upper subtidal from the north regions of the Barents Sea ecosystems which are more stable envi­ (Karasev, 1988). In the more low­ ronments than the littoral ones. Bivalves latitude Arctic regions the proportion of and polychaetes are involved as interme­ trematodes increases in the seabird diate hosts and in particular near the helminth fauna. Some of these tremato­ Greenland coast, G. somateria meta­ des belong to the "pygmaeus" group -M. cercariae are recorded in the bivalve pygmaues, M. pirifirmes and M. trian­ Hyatella arctica (Petersen, 1985). In the gulatus, with autonomic life cycles North Sea in winter G. choledochus and involving the Arctic-boreal mollusc, L. G. deliciosus cercariae do not leave saxatilis. In eiders and gulls at the south molluscs (the first intermediate hosts) island of the Novaya Zemlya archipela­ but encyst inside the daughter sporocysts go, East Greenland and South Spitzber­ (Loos-Frank, 1969; Lauckner, 1983). gen, gymnophallids such as Gymnop­ Thus, their life cycle becomes comple­ hallus somateria, G. choledochus and G. tely autonomous. Most probably, com­ deliciosus (Levinsen, 1881; Odhner, pletion of gymnophallid life cycles in the 1905; Markov, 1941; Brinkman, 1975; Arctic coastal zone follows this pattern. 43

Beaming this in mind it is worth noting the Arctic inhabit the boreal zone as that near the Franz Josef Land archi­ well. So, Alcataenia campilacantha is pelago we did not record any gymno­ recorded in guillemots at the Franz Josef phallids in eiders or in sublittoral bival­ Land, Novaya Zemlya, Greenland, Kola ves including H. arctica. coast, Iceland, North America (Markov, The trend towards an increase in 1941; Belopolskaya, 1952; Baer, 1956; trematode species continues further in 1962; Threlfall, 1971; Hoberg, 1986). the sub-Arctic regions. We have already The same is true for Te trabothrius discussed features of this process, and as erostris and Microsomacanthus ducti/is a result, trematodes become the predo­ in gulls, A. armillaris in guillemots and minant component of helminth fauna of others. coastal birds in regions of moderate Due to interregional and sometimes climate (Lauckner, 1985). local differences in the birds' diets, Species diversity of acanthocephalans values for prevalence and parasite load and cestodes, especially of hymenolepi­ change from region to region. As only dids, also increases in these areas. scanty data is available we are unable to However, almost all species recorded in suggest which features of the life cycles

Table 5. Composition of the helminth fauna of Seven Island archipelago seabirds in 1991-1994 (our data) and in 1940- 1941 (Beloposkaya, 1952)

Bird species No of Trematoda Cestoda dissected Prevalence Intensity Prevalence Intensity birds % (maximal) % (maximal) 't) l-'94 '91 -'94 '91-'94 '91-'94 '91 -'94 ('40 -,41) ('40-' 41) ('40 -,41) ('40 -,41) ('40 -,41)

Herring gull 19 (25) 15.8 (80.(}) 15 (56) 84.2 (1OO.o) 48 (5 1) (Larus ar/;entotus) Great black-backed gull 6 (23) 0.0 (60.8*) (} (237*) 50.0 (82.6) 9 (76) (Larus marinu.1) Kittiwake 29 (38) 27 .6 (32.0) 5 (10) 69.0 (65.9) 110 (61) ( Rissa I rida!'lylo) Black guillemot 6 (22) 0.0 (18.6) (} (27) 50.0 (54.5) ll (15) (Cepphus ;;ri//e) Common guillemot I 0 (50) 0.0 (2.0) (} ( 4) 0.0 (36.0) 0 (9) (Uria aal;;c) Brunnich' s guillemot 11 ( 14) 0.0 (7 .1) 0 ( 1) 27.3 (64.3) 2 (14) (Uria lomvia) Puffin 13 (26) 0.0 ( 11.4) 0 ( 4) 7.7 (23.1) 1 (I) ( Fratercula orctil'll) Razorbil 12 (22) 0 (0.0) 0 (0) 0.0 (18.2) 0 (2)

(Alca torda) * - Cryptocoty/e linguo prevalence and maximal intensity are pointed out because summary trematode prevaknce and i ntensity in the great black-backed gulls is not given by Belopolskaya

(1952). Bes ides C. lingua, this bird was infected 25 .8% with Gymnophallus deliciosus 44 of the above-mentioned parasites, con­ trematodes which were only represented tribute to their distribution. There is no with 2 species ( Cryptocotyle lingua and question that absence of free-living Gymnophallus deliciosus) in the archi­ larvae, involvement of the common pelago seabirds investigated in 1991-93 arctic-boreal crustaceans (for example, in comparision to 11 species recorded by euphausiids) and fishes and the high Belopolskaya in 1940-41. From the fecundity which is typical for all mature richest (9 species, 1940-41) trematode cestodes, play a part in this. All together, fauna which was that of the herring gull, these features may decrease to some such common species as C. lingua, extent dependent on limiting factors in Microphallus similis and Renicola mur­ both the macro- and microenvironment. manica, have disappeared. These life cycles are capable of comple­ Changes recorded in the cestode tion over the whole distribution area of fauna of the archipelago seabirds were the final hosts (seabirds). not so conspicuous and can be contribu­ 4. Life cycles and seabird helminth ted mainly to changes in these diets. The fauna under changes of the ecological change of priorities of fish species conditions foraged could have provoked the disap­ pearance of Tetrabothrius cylindraceus The above-listed features of the life and the simultaneous increase of infecti­ cycles, which are to a certain typical for on with T. erostris (in herring gull: from all seabird cestodes, contribute to their 23.5% in 1940-4 1 up to 73.7% in 1991- high resistance to any changes in ecolo­ 93) and the inclusion of T. immerinus in gical conditions. In 1991-93 we carried the tetrabothriid fauna. The increase in out parasitological observations on the the proportion of small crustaceans seabirds' colonies at the Seven Islands (Mysidacea, Euphausiacea, Calanoidea) archipelago (Eastern Murman) utilising in kittiwake diet may have caused an in­ the methods and in the seasons adopted crease (from 41.1% to 69%) of infection by Belopolskaya (1952) in 1940-41. with Alcataenia larina. At the same time Over the past 50 years since Belopol­ this species disappeared from the herring skaya's studies, the number of seabirds at gull helminth fauna whereas Wa rdium the archipelago and their food composi­ cirrosa appeared, and infestation with tion have changed essentially due to Alcataenia micracantha and Micro­ anthropogenic influences. Due to fishery somacanthus ductilis, increased. Most activities, the proportions of herring probably, that was preconditioned by the ( Clupea harengus) and capelin (Mallotus increase in the quota of the littoral and villosus) have dropped sharply whereas upper sublittoral crustaceans (intermedi­ proportion of sandeel (Ammodites tobia­ ate hosts for the above-listed cestodes) in nus) and also the cod (Gadus morhua), herring gull diets, as compared to 1940- redfish (Sebastes spp.), goby (Myoxo­ 41. cephalus scorpius), etc. have increased in the food composition of fish-eating In our opinion, the sharp impove­ seabirds (Krasnov et al, 1995). The rishment of the trematode fauna results analysis of the seabird parasite fauna to a great extent from the decrease in the revealed its apparent qualitative and number of their principal final hosts - the quantitative impoverishment (Galkin et herring gulls, great black-backed gulls al, 1994; Galaktionov, 1995) (Table 5). and common gulls in the archipelago This trend was especially obvious for area (Krasnov et al, 1995). It has been 45 mentioned earlier that the East Murman ving I or 2 free-living larval stages. At is the northeastern boundary of the the same time local foci of infection by known distribution area of trixenic these species may be found in regions trematodes possessing I to free-living where environmental conditions appear larvae. Their prevalence in the first inter­ to be generally unfavourable for com­ mediate host (molluscs) in this area is pletion of their life cycles. thus extremely low in comparison to 4. Presence of free-living larvae and western parts of the Barents Sea coast use of boreal molluscs as first interme­ (Galaktionov & Bustnes, 1996). Its fur­ diate hosts prevents the advance of ther decrease in the archipelago area, as seabird trematodes into the Arctic. At a result of the decrease in the main the same time the conditions are favou­ species of final hosts, should lead to an rable for the completion of the autono­ even greater decrease in the possibility mic life cycles of cestodes and a­ of infection of the second intermediate canthocephalans. This is also promoted hosts. As a re sult, the possibility of a by a high proportion of crustaceans in gull eating a mollusc containing invasive the diet of Arctic seabirds. In boreal metacercariae, becomes extremely small. regions trematodes become the predomi­ Conclusions nating component in the helminth fauna of the seabirds. The analysis conducted has provided the following conclusions: 5. Environmental change in sub­ Arctic coastal waters is a primary factor l. In coastal ecosystems the life influencing trematodes parasitizing sea­ cycles of the seabird trematodes, acan­ birds because this region is the north­ thocephalans and some cestodes are eastern limit of the distribution area of completed due to their close association these trematodes. Composition of sea­ with the benthic invertebrates in these bird cestode fauna is less vulnerable to environments. At the same time, Tetra­ fluctuations. Change in feeding priorities bothriidea and some Dilepididae (Alca­ by seabirds is the most important factor taenia) which use pelagic plankton influencing trematode and cestode crustaceans, ccphalopodcs and fishes as infections. their intermediate hosts, can complete their life cycks in the open sea. 6. The analysis provided clearly demonstrates the necessity for more 2. The richest helminth fauna is thorough studies of seabird parasite life recorded in seabirds (waders, eiders, cycles, knowledge of which is far from gulls) feeding on the littoral and upper perfect. sub littoral in vertebrates. The poorest is recorded in spcciali;A�d fi sh-caters (some Acknowledgements gulls, guillemots and petrels) and plank­ I wish express my gratitude to Dr. tonphagous bird (little auk). S.W.B. Irwin (University of Ulster) for 3. In the Arctic and sub-Arctic coastal his valuable advice and improvement of ecosystems scabird trematodes with the English version of the manuscript. autonomic dixcnic life cycles (micro­ References phallids or the "tl)lglllaeus" group), pre­ dominate. In the borcal regions, due to Baer JG. Parasitic helminths collected in competition, they give up their place to West Greenland. Medd Gronland 1956; 124: species with trixcnic life cycles invol- 1-55 46

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IMPACT OF SEABIRD HELMINTHS ON HOST POPULATIONS AND COASTAL ECOSYSTEMS

K.V. Galaktionov Murmansk Marine Biological Institute, Murmansk, Russia1

Abstract Death of seabirds as the result of dus (Kulachkova, 1953, 1960, 1979; helminth infections has been described Grenquist et al., 1972; Person, 1974), in the literature many times; recently a trematodes Paramonostomum alveatum comprehensive review was undertaken and microphallids of the "pygmaeus" by Lauckner ( 1985). Almost all referen­ group (Kulachkova, 1960, 1979; Person, ces are devoted to marine ducks 1974). Lauckner ( 1985) described death (especially eiders) and gulls. These of common gull due to heavy infection seabirds are closely connected with with the trematode Cryptocotyle lingua. coastal ecosystems, where life cycles of Renicolid trematodes parasitizing kid­ most helminths are completed (Galak­ neys of seabirds, especially gulls, also tionov, this volume). Heavy infection cause some pathological effects (Hill, with intestinal helminths may cause 1952, 1954; Wright, 1956; Riley & intestinal haemorrhage, destruction of Wynne Owen, 1972; Sudarikov & Sten­ large areas of intestinal mucosa, hypera­ ko, 1984). emia, enteritis, dilation of tissues and All the above-mentioned helminths, intestinal blood vessels, etc. Acantho­ as well as many others, are usual com­ cephalan infections result in emaciation ponents of bird parasite fauna and only and development of fibrous capsules cause death of birds when heavy infecti­ involving the submucosa and muscular ons occur. There is, however, seldom layers, with occasional penetration of the any convincing evidences that death of intestinal wall resulting in peritonitis. birds is the direct effect of helminth Among the most pathogenic helminths parasites. As Thompson (1985) has causing death of common eiders are the noted, most investigators arrive at this acanthocephalans Profilicollis botulus conclusion following the discovery of and Polymorphus minutus (Belopol­ dead birds which are heavily infected skaya, 1952; Thorn & Garden, 1955; with helminths. At the same time, they Clark et al., 1958; Garden et al., 1964; pay no attention to dead birds which are Grenquist, 1970; Persson, 1974; Itamies found devoid of helminths or containing et al., 1980, etc.), cestodes Microsom­ few of them. Comparisons of infection acanthus spp. and Schistocephalus soli- levels of seabirds found dead and those

1 Current address: Zoological Institute, St Petersburg, Russia 51 taken alive are very seldom given. A Even greater uncertainty appears study of this type carried out on the after attempts to evaluate helminth Ythan Estuary (Scotland) (Thompson, influence on host populations, especially 1985) revealed no significant distinction taking into account that such studies of in the intensity of infection with the seabirds are extremely rare. I am going acantocephalan P. botulus between to consider some aspects of this pro­ common eiders from the two groups blem, especially as it applies to coastal compared. Nevertheless, according to ecosystems of notthern seas. Persson et al. (1974), in Sweden only 28% of common ciders taken alive were 1. Helminth impact on the White Sea common eider population in a poor state of nutrition or emaciated compared with 93ri{J of common eiders Substantial data on the helminth found dead. Most of those seabirds impact on the White Sea population of suffered from enteritis resulting from common eiders were obtained by Ku­ heavy trematode infection. lachkova (1953, 1958, 1960, 1979) in the

1949 !950

!95! J952

Fig. 1. Percentage of co mmon eider nestlings death associated with different helminth species in the Kandalaksha reserve in 1949-1952 (after Kulatchkova, 1953)

Microphallids of the "pygmaeus " group; Paramonostomum alveatum ; Ill- -

complex infection: Parmnonostomum alveatum + microphallids of the "pygmaeus " D-group + Microsmnacanthus spp.;

""" Micro.1·omm·unthus spp.; v"v"• - non-parasitic reasons. j:::::'.:l- v " 52

Kandalaksha reserve (Kandalaksha Gulf, etc.) they become infected with helminth the White Sea). Monitoring of the com­ larvae. In the Kandalaksha Gulf the most mon eider population has been carried pathogenic helminths are trematodes, out there since 1935; in 1950-1980 it Paramonostomum alveatum; microp­ was accompanied by a parasitologica1 hallids of the "pygmaeus" group and study of the seabirds. The investigations cestodes, Microsornacanthus spp. revealed that helminth infections mainly (Kulachkova, 1960, 1979). The number influenced the nestlings, especially of nestlings which perish due to different during the first two weeks of their life. parasites varies from year to year (Fig. This is a critical period for common 1 ). Probably this is connected with eider nestlings (Kmjakin, I 987) and by differences in levels of infection of feeding only on littoral invertebrates intermediate hosts from year to year, (periwinkles Littorina spp. , mainly) local differences in sites of nestling (Bianki et al., I 979; Kmjakin, 1989; foraging, etc.

Fig. 2. Life cycle of Paramonostomum alveatum (after Ku1atchkova, 1961)

I - adult in the common eider's intestine; 2 - eggs; 3 - first intermediate host - Hydrobia ulvae; 4-redia; 5 - developing cercaria; 6-fully-fo rmed cercaria in water; 7-8 - cercariae encysted (ado1escariae) on the shell of H. ulvae and Littorina sp. 9 - adolescaria.

P. alveatum rediae develop within host by the invasive larvae. According to littoral molluscs Hydrobia ulvae; after Kulachkova's calculations ( 196 I), one leaving the molluscan hosts the cercariae hydrobia shell can carry up to 260 cysts encyst on the surface of shells of hydro­ of P.alveatum adolescariae. Heavy infec­ bians, periwinkles, mussels (Fig. 2). As tion of nestlings is also promoted by the it has been mentioned earlier, these fact that mass release of P.alveatum molluscs form the main forage base of cercarie from the molluscan hosts coin­ nestlings. Subsequently this ensures a cides with increase of water temperature high probability of infection of the final up to 23-26 °C in pools retained in the 53 tidal zone during low tide (Kulachkova, 1961). This takes place at the end of June - beginning of July, i.e. in the period when common eider nestlings begin to forage in the tidal zone. At roughly at the same time an increase of the infection of periwinkles Littorina spp. with invasive metacercari­ ae of microphallicls of the "pygmaeus" group is recorded (Galaktionov, 1985, 1992). These larvae are formed within daughter sporocysts (Fig. 3), the number of metacercariae in one infected mollusc can reach 7600 (Belopolskaya, 1949). As a consequence of their development, the behaviour of the infected molluscs is changed (Galaktionov, 1993). Molluscs containing sporocysls with invasive Fig. 3. Life cycle of "pygmaeus" group metacercariae creep to open places microphallids (surface of stones, algal tips etc.) (Fig. ingestion of littoral amphipods Gam­ 4), where lhL�Y become available for marus spp. (the intermediate hosts of young eiders. Thus the probability of life this parasite). Even at a rather low cycle completion is gn�at ly increased . prevalence of crustaceans (up to 9% ), Infection of' yo1111g eiders with the infection intensity can reach 250 Microsomacanthus SflfJ. lakes place after specimens per amphipod (Kulachkova &

Lilforina ohtusa/,1 Littorina saxatilis

Prevalence (%) of

sporocysts youug sporocysts young with fu lly sporocysfs with fu lly sporocysls fonncd formed metaccrcari:w met accrcari ae

52,9 I

13,5 1 1,4() 46,7 + 6,44 11,7+4,15

8,2 I 2,4H 10,7 I 2,HO 28,4 + 4,07 33,3 +4,25

Fig. 4. Distribution of periwinkles infected with "p ygmaeus" microphallid daughter sporo­ cysts of dif'fcn�nt age along the seaweed frond during the high tide (after Galaktionov, 1993) 54

Bityukova, 1980; Marasaeva, X 1()()() 1990). This may be due to the 9 fact that whole gravid proglot­

tids are eaten rather than a· individual eggs. The above-mentioned life cycle features promote heavy

infection of young eiders with m -6 the helminths under conside- t;� ration. According to Ku- 5 lachkova's data (1958, 1960, 0 1979) obtained in different f2 years, the intensity of infection � 4 with P. alveatum in the nest- z lings found dead reached 50 000 specimens per bird (average number 10-12 000), with "pygmaeus" microphal- .- ... ' ' lids - tens of thousands of I \ specimens (up to 639 540), with Microsomacanthus spp. -

in a range from several hund 1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 reds up to tens of thousands of Fig. 5. Long-term changes in number of common eider specimens (the recorded maxi­ nests in the Kandalaksha reserve (Kandalaksha Gulf of mum 54,880). Experiments the White Sea) (after Karpovich, 1987) carried out by Kulach­ kova(l953) have shown that adverse Karpovich, 1983; Karpovich, 1987). effects of parasites became obvious at This corresponded to the years in which much lower values of intensity in nest­ the maximum number of seabirds nes­ lings. In one of those experiments, each ting in the Kandalaksha Gulf was repor­ eider nestlings ( 1 day old) ate 600 P. ted (Karpovich, 1987) (Fig. 5). Probably, alveatum adolescariae. The infected and the increase of their number in the 1970s control nestling groups were kept under resulted in the increase of infection of the same conditions for 18 days. In the intermediate hosts. In the tidal zone, control seabirds body mass increased by foci of infection arose and provoked an 159 g and in the infected ones by 70 g. epizootic in 197 6-1977. Following this a The average daily increase was up 9.3 drastic decrease in the number of birds and 4.1 g, respectively (Kulachkova, nesting in the Kandalaksha Bay took 1953, 1960). place. The decrease continued till 1985 Dead, common eider nestlings, when the trend changed to an increase of heavily infected with helminths are common eider. Unfortunately, this recorded every year at the coast of the elevation in bird number was not accom­ Kandalaksha Gulf. The largest mass panied by a parasitological study. Ku­ death was recorded in 1976-1 977, when lachkova ( 1960, 1979) recorded the 90% of all nestlings were assumed to deaths of significant numbers of eider perish from helminthosis (Bianki & nestlings from helminthosis in the 1950s, 55

i.e. during the second (fig. 5) increase in · tions, at the White Sea common eider the Kandalaksha reserve of the common nestlings which are weakened due to eider numbers. various reasons (including helminthoses) The data presented suggest that arc the main victims of large gulls. At helminths can significantly influence the the south-eastern coast of Australia mass dynamics of the number of White Sea death of Little Penguins (Eudyptula common eiders. Moreover, the helminths minor) is recorded regularly. In 1986 can influence the whole population about 2 000 birds were found dead rather than just a local one. According to (Norman et al., 1992). All of them were the current data (Km:jakin et al., 1988), heavily infected with trcmatodcs, cesto­ common eiders at the White Sea consti­ dcs and nematodes; the infection caused tute a separate population which spends pathology of the internal organs of the the entire year on the White Sea and birds studied. In the authors' opinion winters in polynias. The main nesting (Norman et al., 1992), annual variations sites are on the islands in Kandalaksha in the incidence of parasites and their Gulf and Onega Gulf. effect may have been related to food (= intermediate hosts) abundance and/or 2. The extent of helminth impact on availability. The parasites' influence may seabird populations be intensified in periods of storms. Unfortunately, examples of simulta­ We suggest that the effect of parasi­ neous ornithological and patasitological tes at populational level consists of a monitoring carried out over a number of decrease of bird resistance to other years and similar to the one already unfavourable factors. In this respect it is described arc uniqm�. J\s a result, it is similar to the influence proposed for impossible to give a gent�ral evaluation anthropogenous pollutant accumulation of the extent or parasite influence on in the tissues of scabirds (heavy metals, scabird populations. Based upon avai­ chlorinated hydrocarbons, etc.). Ne­ lable literature rdcn.,nccs concerning vertheless, a premium is placed upon other groups of hosts (Kennedy, 1975; investigation of the characteristics of Anderson, I 979; Madscn, 1981; Scott & pollutant distribution in marine ecosy­ Dobson, 1989 etc.) we can suggest a stems and these studies get substantial priori that the., d c., gree of this influence financial support. Parasitological work, may be quite high. Moreover, under on the other hand, attracts little attention normal conditions helminths do not and less support. Really, we have next to directly cause the deat h of scabirds. If no information on the current compositi­ the host-parasitt', ha lanCL', is disturbed, for on of the scabird parasite fauna on the example by an incn.,asc in fi nal host coasts of Europe. Only a few studies numbers leading to an extensive increase have been carried out at population in infection of intt',rmcdiate hosts, this level. can lead to a drastic decrease in final At the same time, in recent decades host numbers in subsequent years. human actiVIties have significantly At the sanw tillll'-, as was shown by changed ecological conditions in seas, Skorping (I<)<)(,) hL',Iminths can affect the especially in coastal zones. Trophic reproduction success of common eiders. connections of scabirds have changed Probably in1portant is the birds wea­ and this has inevitably resulted in chan­ kening due to the helminth infection. So, ges of parasite fauna composition according to Korjakin's (I 987) obscrva- (Galaktionov, 1995; this volume). 56

An event as remarkable as the mass which is caused by extensive fresh-water death of guillemots during wintering on runoff in the spring, results in mass the Barents Sea in 1986-1 987 (Vader et death of littoral periwinkles Littorina al., 1990) was ignored by parasitologists. spp . Dissection of these molluscs has In summer of 1987 only 10-16% of the revealed that 60-80% of them are infec­ common guillemots and 53-56% of ted with microphallids of the "pygmae­ Brunnich's guillemots, as compared to us " group (Galaktionov, 1992). One of 1986, were recorded in colonies of the the most common effects of the influen­ Norwegian and Kola shores of the Ea­ ce of trematode parthenites on molluscan rents Sea and the Bear Island (V ader et host is castration by parasites (Baudoin, al., 1990; Krasnov, 1990). The main 1974; Sousa, 1983; Minchella et al., reasons of this massive decrease in 1985; Dobson, 1988 etc.). Consequently, numbers was starvation due to the drastic the infected specimens become an decrease in capelin resulting from fis­ "ecological ballast". They participate in hing, combined with severe climatic the intra-specific competition for food, conditions in the winter of 1986-1987. It refuge and so on, but have no reproduc­ was suggested that accumulation of tive importance ( & Hurd, 1983; pollutants in bird tissues also played a Galaktionov, 1985, 1993). partial role, but no attention was paid to Impacts of this sort must be exhibi­ parasites. ted at the population level. However, 3. Impact of seabird helminth larvae their character depends on both the on populations of coastal invertebrates specific relationship features in each host-parasite system, and the intensity of The problem of seabird parasites has infection by parasites in the intermediate another, more large-scale, significance host population. In Littorina spp. popu­ for coastal ecosystems as a whole. It has lations, which have recently been studied been mentioned (Galaktionov, this over several years on the Barents and volume) that most seabird parasites, as White Seas, no obvious effects were they utilise invertebrates from the littoral revealed in spite of their quite high and upper sublittoral zones as interme­ infection level with "pygmaeus" group diate hosts, are connected with these microphallids (Galaktionov, 1993; Gra­ ecosystems. Impact caused by helminth novich & Gorbushin, 1995). In the larvae or parthenogenetic generations (in White Sea populations of L.saxatilis the case of trematodes) may be quite which were heavily infected, female significant (J ames, 1965; J ames et al., fecundity is higher than in less infected 1977; Lauckner, 1980, 1984, 1985, 1987 populations living under similar conditi­ etc.). ons (Granovich, 1992). Similar results As a rule, infection with trematode were noted in the periwinkle population parthenites and larvae results in the inhabiting brackish zones of the coast decrease of molluscs' resistance to unfa­ where elimination of young specimens vourable environmental factors: external was significant (Atkinson & Newbury, temperatures, salinity fluctuations and so 1984). on (Vernberg & Vernberg, 1963; Another type of effect has been Tallmark & Norrgren, 1976; Souse & revealed in some populations (Galak­ Gleason, 1989; Galaktionov, 1993 etc.). tionov, 1985; Granovich,l 992). It is due So, reduced salinity of the superficial to different infections of male and fe­ water layers in the Barents Sea bays male periwinkles of different ages. In the 57

young molluscs, the age-dependent in­ little reproductive importance. They take crease of infection is the same for males virtually no part in population reproduc­ and females whereas it stops or tends to tion. decrease in the older females, and beco­ A high mollusc resistance against mes greater in older males (Fig. 6). The trematode infection in the first breeding females in the older age groups exhibit season was observed in L. littorea po­ the greatest individual fecundity, and pulations at the British Isles (Robson & according to ourdata, they contribute up Williams, 1971). These molluscs are to 40-50% of the total fecundity of the responsible for the reproduction of the Barents Sea L saxatilis population periwinkles whereas the older specimens (Galaktionov, 1985; 1993). In contrast, are infected heavily with trematode males from the older age group have parthenites of different species (Robson

INFECTION

·;. IUO

90

BO _-

-_ 70

60 -.. · ·· · · ·· - �- ...... � 50 · I 40 :_

30 :-

20 :_

10 ·�

0- " 6 7 8 10 ll SHELL HEIGHT

INFt:CTION INFECTION % 0 - 9 % l3

JO

sm:LI, HEIGHT SHELL HEIGHT

Fig. 6. Trematode infection of male and female periwinkles Littorina saxatilis of different size­ age groups (distinguished on the base of shell height) in different populations of the Barents Sea coast (after C!alaktionov, 1993)

a-Yarn ishnaya Bay (eastern Murman); b-Big Zinkoviy islet (coast waters ofVajgatch island);

c-Krasniy islet (coast waters of Vajgatch island). 58

& Williams, 1971; Hughes & Answer, the Welsh coast in winter of 1973-74 1982). Certainly, other still unknown resulted in increased infection of mol­ mechanisms contributing to the relati­ luscs Scorbicularia with Meiogymnop­ vely ineffectual influence of trematode hallus minutus parthenites. This parasite parthenites and larvae on intermediate uses these birds as final hosts. As a host populations are likely to exist. This result a mass death of cockles (the would not be surprising, taking into second intermediate hosts) took place consideration the duration of the eo­ due to the over-infection with metacerca­ evolution of al l the components of host­ riae (lames et al ., 1977). The extent of parasite systems. examples like these may be greater than But all these mechanisms are only of realised. However, it should be noted value up to a certain critical level. By­ that good intentions (such as the total per-infection of intermediate host popu­ protection of seabirds) can result in lations can result in their destruction. In dangerous consequences for populations North Sea populations of L. littorea of coastal invertebrates. having a high intensity of infection, the 4. Increase in gull numbers and its phenomenon of "zero growth" was probable effects on the coastal ecosy­ observed. This was due to the death of stems of northern seas the large molluscs as a result of tremato­ As a result of protection, increase in de infection (Lauckner, 1987). This gull numbers (herring gull, great black­ contrast with coastal regions where backed gull, common gull) has been periwinkles are only lightly infected. known to take place. At the same time a Here a decrease in the number of L. litto­ reduction of the traditional food source rea veligers in the plankton is recorded. (fish) of these seabirds is recorded, due In some regions of the North Sea coast to intensive fi shing. As gulls are euryp­ where infection of periwinkles with the hagous birds, they begin to search for trematode Himasthla elongata is high, food in the anthropogenous landscape the larvae damage populations of the and accumulate alongside coastal settle­ second intermediate host (molluscs ments. In 1950-60s herring gulls and My tilus edulis and Cardium edule) great black-backed gulls were only (Lauckner, 1984). Even relatively light recorded near Murmansk in the Kola infections with metacercariae cause Bay. Since 1975, due to the devastation death of young cockles, and their accu­ of herring resources in the Barents Sea mulation in the older specimens results and Norwegian Sea they have been in mass death in the third summer of appearing near dumps and fur farms. their life - this effect is referred to as This phenomenon became common in "summer mortality" (Lauckner, 1984). the beginning of 1980s, due to a great It should be stressed that the most reduction of capelin. In that period a important factor which results in the decrease in the number of large gull mass infection of intermediate hosts is colonies was observed on the islands of increase in the concentration of final the Murman coast (Krasnov et al., 1985) hosts. It follows that, in the above case, whereas the seabird accumulations near foci of invertebrate infection in North Murmansk reached tens of thousands Sea coasts were formed at sites of gull (Paneva, 1989). concentration. Unexpectedly a sharp The large gulls were concentrated in increase in the oystercatcher numbers on regions close to the fishing towns, fish- 59

factories, etc., where the seabirds feed on onov, this volume). An increase in waste from fishing activity. There high capelin and sancleel numbers in the concentrations of gulls accumulated in Barents Sea was accompanied with the quite small sections of coastline, and this appearance of the largest accumulations promoted favourable conditions for the of large gulls in Europe (Ban·ett & completion of helminth life cycles. It is Vacler, 1984; Furness & Ban·ett, 1985). not surprising that an increased infection In the course of our work in September, of littoral invertebrates with helminth 1994, we noted large accumulations of larvae is recorded in such places these birds in areas associated with (Matthews et al., 1985). fishery activity. We conducted a parasi­ An informative study was carried out tological investigation of the littoral by myself and Dr. J .O.Bustnes on the molluscs, Littorina spp. which we coast of North Norway (from Varanger­ sampled from fishing villages, close to fj ord at the east to Troms0 at the west) fish processing factories, near fish farms and natural sites (controls) within a few (Galaktionov & Bustnes, 1996; Galakti- km from centres of fishery activity.

Llttorlna saxatllls 15 c::::J Control � Fish Industry/farming :0 Q) 12 'U -Q) .E 9 c Q) 0 c 6 Q) iij > ..Q) 3 a..

0 M pygmo..., M.plrilonnet M.llmllil C.llnguo A- Himuthla P.alomOn 18 llltorlna llllorea c::::J Control � :0 15 Fish Industry/farms -Q) 0 .!!.? 12 .E � l!- 9 Q) 0 c �Q) 6 e Q,. 3

0 M.pygmaeua M.llimilil C. lngua Renlcola P.atomon

Trematode apeclea

Fig. 7. Prevalence of different trematode species in periwinkles Littorina saxatilis and L. littorea sampled from areas associated with fishery activity (fishing villages, close to fishing processing factories, fish farms) and natural sites (control) on the coast of North Norway (after Galaktionov, Bustnes, 1996) 60

Analysis of the data obtained from the organism level and can provoke sites of fish industry and fish farming, degeneration of coastal ecosystems near and comparison of these data with those settlements. obtained in control sites, demonstrated This problem has already been the following. There was an increased considered in the literature (Lauckner, infection of periwinkles with parthenites 1985), but no special studies have been and larvae of Microphallus piriformes, carried out. As mentioned previously, M.similis and Cryptocotyle lingua - parasites have been overlooked during typical gull parasites in the. sub-Arctic evaluation of anthropogenous influences regions (Galaktionov, this volume) (Fig. on coastal ecosystems. As said earlier, 7) in the areas associated with fisheries. the protection of seabirds is sacrosanct No significant differences in infection by and no attention is paid to the dangerous eider trematodes, such as Microphallus effects of their parasites on populations pygmaeus were observed (Fig. 7). This is of intermediate hosts. There is no signi­ probably because the waste from the ficant information on the combined fi shing industry is not as attractive to influence of parasites and pollutants on eiders as it is to gulls. Eiders' diet usually gull concentrations near coastal villages. consists of benthic invertebrates. The possibility of increase of infec­ Our study (Galaktionov, Bustnes, tion by other seabirds due to its spread 1996) demonstrated that prevalence of from infection foci near coastal villages gull trematodes in molluscs is higher as a has also been overlooked. This is parti­ rule on the shores near fishing industry cularly important because all the trema­ complexes (fishing villages) than near todes associated with gulls show little fish farms. Perhaps this is due to the fact host specificity. For example, C. lingua that in our study we paid no attention to has been recorded from nearly all speci­ the age of farms. In northern of Norway, es of marine and coastal birds (Lauck­ Kristoffersen (1991) found that C. lingua ner, 1985). In addition to gulls, M. piri­ infection in L. littorea close to char fo rmes can develop (though with less farms increased with the age of the success) in eiders and it is one of the farms. C. lingua infection in periwinkles "pygmaeus" group which is pathogenic near farms established less than 5 years to these seabirds. Infection of eiders as ago was not significant. well as of waders can take place during Thus, an increase in infection of their migrations and/or wintering when littoral invertebrates with gull helminth large flocks may feed in locations close larvae in regions of fishing activity has to the fishing industry. Wider distributi­ been well established. Here populations on of infection by some parasites may of invertebrate are constantly subjected also be promoted by the activity of to parasite pressure which may result in intermediate hosts. This is probably the detrimental effects. Moreover, the in­ case for C. lingua, the metacercariae of vertebrates inhabiting these sites are also which develop in fishes. It can't be subject to heavy anthropogenous influ­ excluded that high infections with C. ences such as pollution with oil hydro­ lingua which were recorded in kittiwake carbons, everyday wastes etc. Consequ­ colonies of Hornoya Island (north-east ently, there is a double pressure (both Norway) (Engstrom, 1989) may have parasitic and anthropogenous) which been connected with the adj acent fishery obviously strengthens pathogenicity at harbour at Vardo. 61

Conclusion References 1. The pathogenic effect of helminths Anderson RM. The influence of parasitic in­ on individual seabirds may be manifes­ fection on the dynamics of host population ted at population level. Under high growth. In: Anderson RM, Turner BD, Tay­ infection intensity, reduction in seabird lor LR, eds. Population Dynamics. Oxford: populations can take place due to mass Oxford University Press, 1979: 245-81 death of infected individuals. Usually the Atkinson WD, Newbury SF. The adaptations parasites weaken the birds and this, in of the rough winkle Littorina rudis to desic­ turn, may decrease their reproductive cation and to dislodgement by winds and success, their resistance to unfavourable waves. J Anim Ecol 1984; 53: 93-105 environmental factors, predation etc. Barrett RT, Vader W. The status and conser­ vation of breeding seabird in Norway. ICBP 2. High infections of coastal inverte­ Technical Publication 1984; 2: 323-33 brates by scabird helminth larvae can cause some destructive effects to their Baudoin M. Host castration as a parasitic populations. This effect has been recor­ strategy. Evolution 1975; 29 : 335-52 ded on coasts where high concentrations Belopolskaya MM. Parasite fauna of marine of seabirds, especially gulls, have accu­ waterfowl. Uchenie Zapiski Leningradskogo mulated. Universiteta 1952; 141, ser Bioi, 28: 127-80 (in Russian) 3. The increase in gull numbers, due Bianki VV, Karpovich VN. Current state of to their protection together with reducti­ the common eider in the White Sea and on of their forage base, has resulted in Murman. In: Uspeskiy SM, ed. Reports of the accumulations of these birds near coastal Baltic commission on the birds' migration villages, fish farms, fi sh harbours etc. studies. Tartu: Estonian Academy of Scien­ This in turn, has resulted in the increase ces Publishers, 1983: 55-68 (in Russian) of infection of coastal invertebrates with Bianki VV, Boyko NS, Ninburg EA, Shkla­ gull helminth larvae. These invertebrates revich GA. Feeding of common eider in the are subjected to double pressures: those White Sea. In: Uspenskiy SM, ed. Ecology of parasites ami 111an made pollution. and morphology of eiders in the USSR. Moscow: Nauka, 1979: 126-70 (in Russian) 4. Format io n of infection foci near coastal villages can negatively influence Clark GM, O'Mera D, Weelden JM van. An populations of littoral and upper sub­ epizootic among eider ducks involving an littoral invertebrates and populations of acanthocephalan worm. J Wild! Manage coastal birds. In other words, the entire 1958; 22: 204-5 coastal ecosystem is affected. Taking Curtis LA, Hurd LE. Age, sex and parasites: into consideral ion 1 hat large gull popula­ spatial heterogeneity in a sandflat population tions and fishny activity arc both incre­ of Ilyanassa obsoleta. Ecology 1983; 64: asing, we can easily predict the effects of 819-28 this in I he lll�ar fut urc. The urgency of a Dobson AP. The population biology of thorough and comprehensive study of parasitic-induced changes in host behaviour. conditions developing in the coastal zone Quart Rev Bioi 1988; 63: 139-65 of Europe is obvious. Engstrom JA. Parasitsamhallem i kyckling hos lunne Fratercula arctica (L.) och hos Acknowledgements tretaig mas Rissa tridactyla (L.): ett kvantita­ I wish to thank Dr. SWB lrwin tivt naermande. Cand Scient thesis i Ecologi, (Ulster University) for comments and Zoologi. Tromso: Tromso University, 1989 correction I he language. 62

Furness RW, Barrett RT. The food requir�­ urn on Littorinid Biology. London: The Ma­ ments and ecological relationships of a lacology Society of London, 1992: 255-63 seabird community in North Norway. Ornis Granovich AI, Gorbushin AM. Differences in Scand 1985; 16: 305-13 the trematode parthenite infection rate in Galaktionov KV. Special features of the males and females of the littoral snail genera infection of the mollusc, Littorina rudis Littorina and Hydrobia in the Kandalaksha (Maton, 1797), with parthenites of Micro­ Bay of White Sea. Parazitologia 1995; 29: phallus pygmaeus (Levinsen, 1881) nee 167-78 piriformes Odhner, 1905 and M. (Odhner, Grenquist R. On mortality of the eider duck 1905) Galaktionov, 1980 (Trematoda: (Somateria mollissima) caused by a­ ) from the White Sea. NOAA canthocephalan parasites. Suom Riista 1970; Techn Report NMFS 1985; 25: 111 22: 24-34 (in Finnish) Galaktionov KV. Infection of males and Grenquist P, Henriksson K, Raitis T. On Littorina females of molluscs of genus (Gas­ intestinal occlusion in male eider-ducks. tropoda, Prosobranchia) with trematode Suomen Riista 1972; 24: 91-6 (in Finnish) parthenites at the Barents Sea coast. Parazi­ tologia 1985; 19 213-9 (in Russian) Hill WCO. Report of the Society's Prosector for the year 1951. Proc Zoo! Soc London Galaktionov KV. Seasonal dynamics of the 1952; 122: 515-33 age composition of daughter sporocyst hemi­ populations of microphallids of the "pyg­ Hill WCO. Report of the Society's Prosector maeus" group (Trematoda, Microphallidae) for the year 1953. Proc Zoo! Soc London in littoral molluscs Littorina saxatilis at the 1954; 124: 303-11 Barents Sea. Parazitologia 1992; 26: 462-9 Hughes RN, Answer P. Growth, spawning (in Russian) and trematode infestation of Littorina littorea Galaktionov KV. Trematode life cycle as (L.) from an exposed shore in North Wales. J components of ecosystems (an attempt of Moll Study 1982; 48: 321-30 analysis by the example of family Micro­ Itamies J, Valtonen T, Fagerholm H-P. Poly­ phallidae). Apatity: Kola Scientific Centre morphus minutus (Acanthocephala) infestati­ Press, 1993 (in Russian) on of eiders and its role as a possible cause of Galaktionov KV. Long term changes of death. Ann Zoo! Fenn 1980; 17: 285-9 composition of the seabirds helminth fauna James BL. The effects of parasitism by larval on the Seven island archipelago (eastern Digenea on the digestive gland of the interti­ Murman). In: Skjolda HR, Hopkins C, Erik­ dal prosobranch, Littorina saxatilis (Olivi) stad KE, Leinaas HP, eds. Ecology of fj ords subsp. tenebrosa (Montagu). Parasitology and coastal waters. Amsterdam: Elsevier 1965; 55: 93-115 Science B V, 1995: 489-96 James BL, Sannia A, Bowers EA. Parasites Galaktionov KV, Bustnes JO. Diversity and of birds and shellfish. In: Nelson-Smith A, prevalence of seabird parasites in intertidal Bridges EM, eds. Problems of a small estua­ zones of the European North coast. NINA­ ry. Proceedings of the Burry Inlet Symposi­ NIKU Project Report 1996; 4: 1-27 um. Univ Coli Swansea. Swansea: Pubis Inst Garden EA, Rayski C, ThornVM. A parasitic Marine Stud and Quadrant Press, 1977: Sess disease in eider ducks. Bird Study 1964; 11: 6, No 1, 1-16 280-7 Karpovich VN. On probable cyclic recurren­ Granovich AI. The effect of trematode ce in the common eider number dynamic. In: infection on the population structure of Lit­ Bianki VV, ed. Problems of the study and farina saxatilis (Olivi) in the White Sea. In: protection of the nature of the White Sea Grahame J, Mill PJ, Reid DG, eds. Pro­ coast. Murmansk: Murmansk Book Publis­ ceedings of the Third International Symposi- hers, 1987: 55-64 (in Russian) 63

Kennedy CR. Ecological animal parasitology. Kulachkova VG. Death of common eider Oxford, London, etc.: Blackwell Scientific ducklings and the reasons determinating it. Publications, 1975 Trudy Kandalakshskogo gosudarstvennogo Korjakin AS. Problems of control for the zapovednika 1960; 3: 91-106 (in Russian) status of populational groups of common Kulachkova VG. Annual and seasonal eider (new aspects of the species study and oscillations in infestation of Hydrobia ulvae unsettled questions. In: Bianki VV, ed. Prob­ with larvae of Paramonostomum alvaetum lems of the study and protection of the nature (Mehlis, 1846) Luhe, 1909 (Trematodes). of the White Sea coast. Murmansk: Mur­ Proceedings of the Karelian Branch U.S.S.R. mansk Book Publishers, 1987: 38-54 (in Academy of Sciences 1961; 30: 79-89 (in Russian) Russian) Korjakin AS. Feeding behaviour of the Kulachkova VG. Helminths as a cause of common cider ducklings. In: Karpovich VN, common eider's death in the top of Kanda­ ed. Ecology of birds of the islands and coast laksha Gulf. In: Uspenskiy SM, ed. Ecology of the Kola North. Murmansk: Murmansk and morphology of eiders in the USSR. Book Publishers , llJS9: 27-40 (in Russian) Moscow: Nauka, 1979: 119-25 (in Russian) K01jakin AS, Krasnov YV, Tatarinkova IP, Kulachkova VG, Bityukova SV. Intertidal Shklarevich FN . On population structure of gammarids as a source of helminth infestati­ the common eider ,)'omuteria mollissima in on for the White Sea fishes and birds. In: the north-west of the USSR. Zoologicheskiy Verbizkas IB, ed. Questions of parasitology Zhurnal 19S2; 6 1 : 1107 -<) (in Russian) of water invertebrates. Vilnijus: Zoological Krasnov YV. Food composition and peculia­ Institute Litvuanian Academy of Sciences, 1980: 57-9 rities in behaviour of gulls by the long-term (in Russian) deficiency of fish forage. In: Karpovich VN, Lauckner G. Diseases of Mollusca: Gastro­ ed. Ecology of birds of the islands and coast poda. In: Kinne 0., ed. Diseases of marine of the Kola North. Murmansk: Murmansk animals. Vol I. Chichester, New York, Book Publishers, I <) l)<): 11-26 (in Russian) Brisbane, Toronto: Wiley, 1980: 311-424

Krasnov YV, Matislwv U

Apatity: Kola Scientific Centre Press, !990: for Cerithidea californica (Gastropoda: Pro­ 76-84 (in Russian) sobranchia). Oecologia 1989; 80: 456-64 Matthews PM, Montgomery WI, Hanna Sudarikov VE, Stenko RP. Trematodes of the REB. Infestation of littorinids by larval family Renicolidae. In: Sonin MD, ed. Digenea around a small fi shing port. Parasi­ Helminths of farming and hunting animals. tology 1985; 90: 277-87 Moscow: Nauka, 1984: 134-89 (in Russian) Minchella DJ. Host life-history variation in Tallmark Bo, Norrgren G. The int1uence of response to parasitism. Parasitology 1985; parasitic trematodes on the ecology of 90: 205-16 Nassarius reticulatus (L.) in Gulmar Fj ord Norman FI, Guesclin PB, Dann P. The 1986 (Sweden). Zoon 1976; 4: 149-54 "wreck" of little penguins Eudyptula minor in Thompson AB . Profilicollis botulus (Acan­ western Victoria. Emu 1992; 91: 369-76 thocephala) abundance in eider duck (Soma­ feria mollissima) Paneva TD. Non-nesting concentrations of on Ythan estuary, Aber­ gulls in the Murmansk vicinity. In: Karpovich deenshire. Parasitology I 985; 91: 563-75 VN, ed. Ecology of birds of the islands and Thom VM, Garden EA. A heavy mortality coast of the Kola North. Murmansk: Mur­ among eider ducks. Fair Isle Bird Observ mansk Book Publishers, 1989: 63-71 (in 1955; 2: 325 Russian) Vader W, Barrett RT, Erikstad KE, Strann Persson L, Borg K, Fait H. On the occurrence KB. Differential responses of common and of endoparasites in eider ducks in Sweden. thick-billed murres Uria spp. to a crash in the Swed Wild! 1974; 9: 1-24 capelin stock in the southern Barents Sea. Stud Avian Bioi 1990; 14: 175-80 Riley .T, Wynne Owen R. Renicola glacialis sp. nov. a new trematode from the North Sea Vernberg WB, Vernberg F.T. Int1uence of fulmar Fulmarus glacialis (L.), with obser­ parasitism on thermal resistance of the mud­ vations on its pathology . .T Helminth 1972; flat snail Nassa obsoleta Say. Exper Parasitol 46: 63-72 1963; 14: 330-32 Robson EM, Williams IC. Ralationships of Wright CA. Studies on the life-history and some species of Digenea with the marine ecology of the trematode genus Renicola prosobranch Littorina littorea (L.). II. The Cohn, 1904. Proc Zoo! Soc London 1956; effect of larval Digenea on the reproductive 126: 1-49 biology of L. littorea. .T Helminthol 1971; 45: 145-59 Scott ME, Dobson A. The role of parasites in regularity host abundance. Parasitol Today 1989; 5: 176-83 Skorping A. Why should marine and coasal ecologists bother about parasites? (This volume). Sousa WP. Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Ha1deman (Gastro­ poda: Prosobranchia) and its trematode parasites . .T Exp Mar Bioi Ecol 1983; 73: 273-96 Sousa WP, Gleason M. Does parasitic infection compromise host survival under extreme environmental conditions? The case Bull Scand Soc Parasitol 1996; 6 (2): 65-89

FAUNAL DIVERSITY AMONG AVIAN PARASITE ASSEMBLAGES: THE INTERACTION OF HISTORY, ECOLOGY, AND BIOGEOGRAPHY IN MARINE SYSTEMS

Eric P. Hoberg Biosystcmatics and National Parasite Collection Unit, Agricultural Research Service, United States Department of /\griculture, 10300 Baltimore Avenue, Beltsville, Maryland, USA 20705

Abstract Systemat ics and parasite biodiversity host switching with minimal cospecia­ provide power and predictability in tion (Alcataenia spp. among Alcidae). In broad studies of history, ecology and contrast, contemporary ecological de­ biogeography in marine systems. Para­ terminants appear more significant as an sitic helminths arc elegant markers of influence on the distribution of digene­ contemporary and historical ecological ans, nematodes and acanthocephalans relationships, geographic distribution among marine birds. Ecologically dis­ and host-phylogeny. Complex life cycles crete assemblages determined by forag­ of helminths arc strongly correlated with ing, prey selection, and distribution are intricate food-webs. I kpcndence on a indicated by patterns of parasite abun­ series of intcnucdiate, paratenic, and dance, prevalence and host range across definitive hosts indicates that each taxonomic, geographic and temporal parasite species represents an array of scales. Thus, knowledge of the evolution organisms within a community and of parasite-host assemblages provides tracks broadly and predictably across direct estimates of the history of eco­ many trophic levels. I lost and geo­ logical associations and community graphic ranges of parasites are histori­ development, and is indicative of the cally constrained by genealogical and temporal continuity of trophic assem­ ecological associations, and these deter­ blages. Parasites constitute probes that minents interact resulting in characteris­ can be applied directly to questions of tic parasite comnnJrlity structure. Gener­ contemporary diversity and the historical ally, the parasite fa unas of pelagic sea­ development of community structure. birds are depauperate, and these are not Concurrently, a predictive framework, indicative of re lietual associations link­ with parasites as indicators, exists for ing marine and terrestrial environments. elucidating the impacts of natural or Some core elements of the marine tape­ anthropogenic perturbations to faunas worm fa una arc archaic and potentially and ecosystems. These concepts and coevolvcd (Tetrabnthriidac and seabird phenomena are examined across a range orders) whereas others have a more of temporal and geographic scales ex­ recent h istorical association emphasizing tending from the North Pacific basin to 66 the Southern Ocean. Parasitology offers extensive geographic ranges, have been the potential to achieve unique insights rare (for Alcidae see: Hoberg, 1984a; about ecological interactions and com­ Threlfall, 1971; for Podicipediformes munity structure over evolutionarily see review by Stock, 1985). The major­ significant time frames. ity of studies were limited temporally Introduction: and geographically, and emphasized a restricted number of avian species at a Seabirds are among the most visible specific locality over a narrow window components of marine biotas, and ex­ of time (e.g. Bourgeois & Threlfall, cluding the Anseriformes, are repre­ 1979; Hoberg & Ryan, 1989; Torres et sented by 6 orders and over 300 species al, 1991 ; also reviewed in Rausch, distributed across the oceans of the 1983). In contrast to most avian groups, world (Harrison, 1983). Marine birds are there is a vast literature dealing with generally highly vagile, secondary and Laridae and particularly large gulls of tertiary predators which occupy specific the genus Larus Linnaeus (e.g. many geographic ranges and habitats and as a reviewed in Bakke, 1972, 1985; Threl­ consequence are excellent indicators of fall, 1966, 1967, 1968), probably re­ the state of marine ecosystems. The flecting the abundance of these birds and marine avifauna has received broad their accessibility for research. Also attention with respect to ecology (e.g. typical, have been studies limited to Ainley & Boekelheide, 1990; Ashmole, particular taxa of parasites including 1971; Bartonek & Nettleship, 1979; cestodes (e.g. Cielecka et al, 1992; Belopol'skii, 1957; Croxall, 1987; Galkin et al, 1995; Odening, 1982), et al, Vermeer 1993a), biogeography nematodes (e.g. Johnston & Mawson, (e.g. Murphy, 1936; Shuntov, 1974; 1942; Mawson, 1953; Tsimbaliuk & Siege!- Causey, 1991 ), and systematics Belogurov, 1964), digeneans (e.g. Be­ (e.g. Cracraft, 1985; Imber, 1985; logurov et al, 1968; Leonov et al, 1965) Livezey, 1989; Murphy, 1936; Siegel­ or acanthocephalans (e.g. Hoberg, Causey, 1988). With rare exceptions, 1986b; Zdzitowiecki, 1985) in a specific parasitological studies have never been a geographic region. Ecologically-based usual component of such research pro­ collections which examined the diversity grams concerning birds in marine sys­ of parasitic helminths occurring among tems (Table I) although it is evident that phylogenetically disparate but sympatric parasites offer substantial information host groups, often representing discrete and insights that otherwise are difficult feeding guilds, have been less common to obtain (e.g. Bmtoli, 1989; Hoberg, in the literature (e.g. Belogurov, 1966; 1986a, 1996; Hoberg et al, 1996). The Belogurov et al, 1968; Belopol'skaya, following comments will be limited to 1952; Hoberg, 1983, 1992a; Galkin et al, current knowledge of the helminthic 1994; Markov, 1941; Smetanina, 1981; parasites of seabirds, although a sub­ Smetanina & Leonov, 1984). stantial body of work on ectoparasites, particularly lice, has been published over The most detailed data for host-range the past century (see Hoberg et al, 1996; and geographic distribution of parasite Mauersberger & Mey, 1993). faunas in seabirds are known for high latitudes of the Holarctic and the South­ Synoptic parasitological studies of ern Ocean, whereas there is a paucity of avian families or orders, based on large comparable data from subtropical and sample sizes of hosts examined across tropical regions. Across the Palearctic, 67

Table I. Species of seabirds examined for helminth parasites.*

Number of Number of species % species examined examined Charadriiformes 119 73 61 Laridae 95 52 55

Larinae 46 31 67

Stcrninae 41 14 34

Stercorarinac 5 5 100

Rhynchopinac 3 2 67

Alcidac 24 21 88

Sphenisciformes

Spheniscidac 16 9 56

Procellariifonllcs 104 32 31

Diomedcidae 13 9 69

Procellariidac 66 19 29

Oceanitidac 21 2 10

Pelecanoididae 4 2 50

Pelecanifo n1ws 62 34 55

Pclccanidac 8 8 100

Sulidac 9 3 33

Phalacrocorm� i< lae 33 15 45

Anhingidac 4 4 100

Frcgatidac 5 3 60

Phaclhonl idae 3 33

Podici pcd i forJlles 21 13 62

Gaviiformcs 4 4 100

TOTAl - 326 165 51

*Based on Jl oherg (IlJ84a), Ryzhikov et al. ( 1985), Schmidt (1986), Temirova and Skrjabin (IlJ n), and Yamaguti (197 1); data for Podicipediformes provided by R.W. Starer. This reflects IIHlSL� species of seabirds from which platyhelminths have been reported, and serves a.'> an index of sampling effort for each avian order. 68 this information has been succinctly A perspective on biodiversity: summarized for piscivorous birds, with a Biodiversity is the result of a com­ large component of these data being plex interaction of phylogeny, ecology, applicable more generally to the Holarc­ geography, and history as determinants tic (for nematodes see citations in Barus of organismal evolution and distribution. et al, 1978; for cestodes and acan­ Diversity within biotic systems can be thocephalans see Ryzhikov et al, 1985). assessed in a number of ways as a func­ Considerable research from the North tion of temporal and geographic scales Pacific, including studies by Russian related to populational, genealogical and investigators were reviewed by Hoberg ecological attributes (reviewed by Ho­ (1984a; 1992a). berg, 1996). Dynamic associations unit­ In the Southern Ocean and Antarctica ing populations through communities are the history of parasitological investiga­ assessed by 1) enumeration of taxa and tions extends to the 1800's coinciding elucidation of interactions within con­ with the earliest explorations in that temporary ecosystems (numerical and region (e.g. Baird, 1853; Fuhrmann, ecological diversity) and 2) recognition 1921; Leiper & Atkinson, 1915). A of monophyletic groups or clades (gene­ series of investigations adjacent to the alogical diversity) leading to cospecia­ Antarctic Peninsula (Hoberg, 1983, tion analyses and documentation of 1987a; and others), particularly those by ancestral areas, regions of endemism, the Polish research group centered in the and significant centers of organismal South Shetland Islands (e.g. Cielecka & evolution. Within this context, historical Zdzitowiecki, 1981; Jarecka & Otas, biogeography and historical ecology 1984; Zdzitowiecki & Szelenbaun­ attempt to elucidate patterns in organis­ Cielecka, 1984; and others), has sub­ mal distribution and macroevolutionary stantially altered our knowledge of processes involved in community devel­ helminth faunas among seabirds inhab­ opment (Brooks & McLennan, 1991). iting this area. Parasitic helminths are elegant indicators These preliminary remarks provide of contemporary and historical ecology, the context for developing an under­ and the long term development of com­ standing of the genealogical, bio­ munities (Brooks et at, 1992; Brooks & geographic and ecological patterns of McLennan, 1993). distribution which characterize assem­ Recent assessments of biodiversity blages of helminthic parasites among have emphasized regions already pro­ seabirds. Consequently, if we are to foundly dominated by anthropogenic define these constituents of biodiversity perturbations and predicted to be of helminth faunas occurring among strongly influenced by climatic change. marine birds, what should be consid­ However, research has often been lim­ ered? Why is this information important, ited in scope taxonomically, geographi­ and what does it tell us about ecological, cally and temporally. This bias has led biogeographic, phylogenetic and histori­ analysis to be largely centered on pi­ cal interactions in marine realms? In scine, avian and mammalian taxa in a essence, why are parasitological data of non-dimensional framework, lacking an significance within the context of orni­ historical context, which has focused on thology, ecology and marine zoology? contemporary communities. Thus, the integrative and interdisciplinary nature 69 of parasitology may add a dynamic assessments of ecological diversity dimension to understanding ecological (numbers of species in a local ecosys­ interactions, patterns of distribution and tem, food-webs, trophic ecology, micro­ the complex history of geographic re­ habitat utilization, patterns of migration gions and biotas, a view long held by and dispersal, biogeography) and com- some parasitologists (Hoberg, 1996). ponents of genealogical diversity (phylogeny, cospeCiatwn, historical Biodiversity and helminths of sea­ biogeography and historical ecology) in birds: specific marine host-parasite assem­ Parasitic helminths, focusing on blages (Brooks & McLennan, 1991; Eucestoda and Digenea, have been Hoberg, 1996). reported from all maj or groups of sea­ birds throughout the world (Tables I, II). Seabird parasites- general trends: In the fo llowing review, Table II has The helminth faunas of seabirds are been used to initially recognize trends in poorly known and represent a substantial distribution and occurrence. This facet of marine biodiversity that has yet "database" is not considered to be ex­ to be evaluated in detail. The majority of haustive, but is tkrivL�d from recent studies of helminthic parasites among compilations (lloberg, I lJX4a; Ryzhikov, marine birds have relied on small, geo­ et al, 19X5; Schlllidl, I lJX6; Stock, 1985; graphically limited collections, and have Yamaguti, 197 1). Jn this manner, a rough focused on descriptions of new taxa or index of diversity can he developed. monographs of specific groups (e.g the Data presented do not reflect evenness, Tetrabothriidae, Baer, 1954; Temirova and are proba bly intluenced by the and Skrjabin, 1978). Although over the degree of sampling t• llort or size of the past 200 years, about 50% of the sea­ avian taxon. However, thL:rc has been no birds of the world (excluding anseri­ attempt to correct fur these variables and forms) have been examined for parasites to more accuratel y reflect species rich­ (Tables I, II) many of these reports were ness (sec Walthc:r 1'/ of, 1995). At a limited to few or single avian specimens primary level , Tables J and II are useful and clearly may not be representative. in I) rccognit ion of general trends in Approximately 234 of about 5,000 distribution and hoshtssociation for known species of tapeworms (5%) have particular taxa of helminths; 2) elucida­ been described or reported from sea­ tion of existing gaps in sampling effort; birds, but many genera are not limited to and thus, in �) identifying where future marine birds. Considering that cestodes studies might bt: focused. often exhibit some level of host­ Initial trends arc� further examined specificity, it is apparent that many using empirical data available for spe­ species remain to be collected and de­ cific avian taxa, parasite groups, and scribed. Additionally, approximately 405 of about 9,000 species of Digenea geographic rc:gions . Such arc requisite in defining whet her apparent host-parasite (4.5%) are known from avian hosts in marine systems. Overall, these data are associations arc real or arlcfactual. At this level the role of parasites in broader erratic in their taxonomic scope, as there studies of marine biodivcrsity will be have been few long term or taxonomi­ explored. Central to this discussion is the cally exhaustive baselines established for a given region or avian group. evaluation of parasites as "biodiversity probes" (Gardner & , 1992) in 70

Table II. Families, genera and species of platyhelminth parasites reported from sea­ birds.*

Digenea Eucestoda Families Genera Species Families Genera Species

Charadriiformes# 24 79 198 5 32 I IO Laridae 24 75 192 5 31 99 Larinae 22 60 145 5 28 87 Sterninae 16 39 80 4 14 33 Stercorariinae 6 6 10 4 7 IO Rhynchopinae 5 7 8 0 0 0 Alcidae 12 14 24 4 9 2I Sphenisciformes# Spheniscidae 3 4 4 3 3 7 Procellariiformes# 3 7 6 2 IS Diomedeidae 1 I 1 2 9 Procellariidae 3 6 6 2 I3 Oceanitidae 0 0 0 Pelecanoididae 0 0 0 Pelecaniformes# 18 60 I4I 4 13 37 Pelecanidae 13 28 44 3 5 9 Sulidae 5 8 9 I 8 Phalacrocoracidae 14 42 68 4 9 19 Anhingidae 9 20 31 2 Fregatidae 3 3 5 2 2 6 Phaethontidae 0 0 0 1 1 I Podicipediformes# 21 45 108 7 33 86 Gaviiformes# 6 15 22 4 1 I 17 TOTAL** 32 122 405 8 54 234 *Based on Hoberg (1984a), Ryzhikov et al. (1985), Schmidt (1986), Stock (1985), Temirova and Skrjabin (1978), and Yamaguti (197 1 ); data for Podicipediformes largely developed by R.W. Storer (unpublished data). #Totals for each order are adjusted to reflect species which occur in multiple host groups (avian families within orders); numbers of species and genera are approximate due to synonomies. **Total number of families, genera, and species from all seabirds. Definable trends in overall "species the most diverse faunas with respect to richness" of helminth faunas among families and species of digeneans and seabirds are evident (Table II). As ex­ cestodes. The grebes also are typified by pected, the Charadriiformes, particularly a highly diverse fauna, with most para­ the Laridae due to their great vagility sites having been acquired in freshwater and eclectic foraging habits in nearshore, environments. In contrast the Procellarii­ freshwater and terrestrial habitats, have formes, although relatively poorly stud- 71

ied, appear to be characterized by a Hymenolepididae and the genus Micro­ depauperate fauna where digeneans are somacanthus Lopez-Neyra, 194 7 con­ rarely observed and only a single family tains species which occur among Laridae of cestodes is represented (Tetra­ and Phalacrocoracidae, but is dominant bothriidae) (e.g. Hoberg & Ryan, 1989). among Anseriformes. Species of Aplo­ Other avian orders fall on a continuum paraksis Clerc, 1903 are found among between these extremes (Table II). the Charadriiformes, including larids and Generally pelagic (oceanic) birds scolopacids, and the Anseriformes support faunas of lower diversity com­ (Spasskii, 1963), whereas those of pared to those found on neritic (over the Wa rdium Mayhew, 1925 are found continental shelf) and littoral (nearshore primarily in larids (Ryzhikov et al, 1985; and shoreline) waters. There should be Spasskaya, 1966). relatively few species of trematodes There are few monophyletic and host­ infecting birds feeding in pelagic and specific groups limited in distribution to neritic zones, due to limitations imposed taxa of seabirds at the ordinal or familial by life cycles of digencans. The major level. Among these, the Amabiliidae and component of the parasite fauna of the genera Schistotaenia Cohn, 1900 and pelagic birds should be cestodes, due to Ta tria Kowaleski, 1904 are core ele­ a broader distribution in oceanic zones ments of the cestode faunas among the for zooplanktonic and piscine intermedi­ Podicipediformes throughout the world ate hosts. Conversely, birds that exploit but are derived from freshwater habitats invertebrates and fishes characteristic of (Schmidt, 1986; Stock, 1985). Consid­ nearshore areas should have both greater ering strictly marine groups, among the numbers of species of trcmatodes and dilepidids, Alcataenia Spasskaya, 1971 cestodes as a re lation of greater prey (9 species) is typical of the alcids and a species diversity and availability. These limited number of Holarctic larids relationships become clear when com­ (Hoberg, 1986a, 1992b) and the mono­ paring the helminth fa unas typical of typic genus Parorchites Fuhrmann, 1921 seabirds. occurs only in antarctic penguins; Distribution of Eucestoda, a brief dilepidids are virtualy absent among overview: procellariiforms. However, the dominant group of cestodes among seabirds is the Principal groups of ccstodes in ma­ Tetrabothriidae. The genera Tetra­ rine birds arc represented by the Tetra­ bothrius Rudolphi, 1819 and Chaeta­ phyllidca, and secondarily by the Pseu­ phallus Nybelin, 1916 (including 42 dophyllidea and Cyclophyllidea. species) are limited to seabirds of 6 Across this fa una, varying patterns of orders and are particularly well repre­ host-association arc evident. For exam­ sented exclusively among marine groups ple, in the Diphyllobothriidae, species of with greatest diversity among the Pro­ Cobbold, 1858, cellariiformes, Pelecaniformes, Charadr­ Schistoceplwlus Crcplin, 1829, and iiformes and Sphenisciformes (Baer, Ligula Bloch, 1782 arc prevalent among 1954; Hoberg, 1989; Temirova & Skrja­ piscivorous birds including larids, gavii­ bin, 1978). forms, podicipcdifonns and some pele­ Typically for hymenolepidids and caniforms (Dubinina, 1966; Ryzhikov et dilepidids, specificity may be manifested al, 1985; Schmidt 1986). In contrast, at the species level for hosts and para- among the Cyclophyllidea, the family 72

sites whereas for tetrabothriids it is at the Paricterotaenia Fuhrmann, 1932, level of avian order. However it is not Lateriporus Fuhrmann, 1907, Wardium, clear, in many speciose genera, whether Aploparaksis, Microsomacanthus, Di­ congeneric species characteristic of a phyl-lobothrium and Tetrabothrius are particular host group are most closely characteristic parasites of gulls (Belo­ related (are monophyletic and form a gurov et al, 1968; Hoberg, 1992a; coevolved clade) or are related to species Hoberg, unpublished data; Sergeeva, occurring among other avian groups 1971; Smetanina and Leonov, 1984). In (indicative of colonization). comparison the fauna of Alcidae is Life cycles of cestodes occurring in depauperate, with only species of Al­ pelagic seabirds are incompletely known. cataenia and Tetrabothrius being typi­ Shimazu (1975) found cysticercoids cal. Similar patterns have been reported identified as Alcataenia armillaris in the Arctic (Galkin et al., 1994). The (Rudolphi, 1810), and A. farina (Krabbe, distinction between these faunas has 1869) from the euphausiid, Thysanoessa both an historical and ecological basis inermis (Kroyer) in the North Pacific. (Hoberg, 1986a). Additionally, when Diorchis pelagicus Hoberg, 1982, may comparing alcids with other wing­ be one of the few hymenolepidids with a propelled divers such as the diving strictly marine life cycle (Hoberg, 1982). petrels (species of Pelecanoides La­ The life cycles of species of cepede, Procellariiformes) and penguins, Tetrabothrius have not been elucidated a similar pattern of low generic-level but are inferred to involve crustaceans as diversity for cestode faunas is apparent intermediate hosts and cephalopods or (Cielecka et al, 1992; Williams et al, fish as second intermediate or paratenic 1974). hosts (Baer, 1954; Hoberg, 1984a, Overall, these relationships empha­ 1987b). The assemblage of intermediate size that patterns of host-association hosts thus would encompass pelagic have been structured by both phyloge­ micro- and macrozooplanktonic crusta­ netic and ecological determinants (e.g. cea, other invertebrates and fishes, and Bush et al, 1990). However more com­ include some groups with relatively plete resolution of the importance of limited vagility (Hoberg, 1995). Addi­ these factors awaits refinement of taxo­ tionally, for many cestodes occurring nomic concepts for genera and species. among larids, some pelecaniforms, Validity of genera and placement at the gaviiforms, and podicipediforms, the generic level for many nominal species source of infection is terrestrial, fresh­ remains uncertain (see Khalil et al, water, or estuarine, rather than exclu­ 1994; Schmidt, 1986). sively marine (see Bondarenko, 1993; Distribution of Digenea, a brief over­ Bondarenko et al, 1987; Matevosian, view: 1963; Ryzhikov et al, 1985; Spasskaya, 1966; Spasskii, 1963). Digeneans with marine life cycles are limited in avian hosts. The major groups, Finally, against this tapestry, it is of based on numbers of genera and species interest to compare avian families within (in order of dominance and richness) are an order. For example, among the Cha­ the Heterophyidae, Echinostomatidae, radriiformes, the Laridae support a fauna Diplostomidae, Strigeidae, Microphalli­ of greater diversity than the Alcidae. In dae, Schistosomatidae, and Renicolidae the North Pacific, species of Alcataenia, (see Yamaguti, 1971). Similar to the 73 patterns of occurrence for cestodes, dige­ be viewed as an endemic focus of para­ neans are rare in birds which forage in sitism. This concept of island-focality pelagic situations (e.g. in most Procel­ explains the potential for interaction lariiformes, Sphenisciformes; Charadrii­ between intermediate and definitive formes- Alcidae). For instance, among hosts linked by trophic associations. the Alcidae many records are repre­ Thus, the diversity of adult helminths sented by single hosts and few speci­ observed should be directly proportional mens of parasites (Hoberg, 1984a) and to the diversity of prey which are poten­ only Pseudogymnophallus Hoberg, 1981 tial intermediate hosts. Moving into is considered to be a typical parasite neritic and oceanic waters, away from an among puffins (Fratercula corniculata island focus, parasite diversity should be (Naumann) and F. cirrhata (Pallas)) and observed to change on a qualitative and auklets (Aethia cristatella (Pallas), A. quantitative basis. The regime of poten­ pusilla (Pallas), Cy clorrhynchus psit­ tial intermediate hosts would be altered, tacula (Pall as)) (Hoberg, 1981). Species as larval parasites become limited in richness and abundance of flukes among their ability to disperse and the feeding some groups such as the Podicipedifor­ adaptations of avian hosts become mes, Pelecanidae, Phalacrocoracidae and specialized for exploitation of select many larids reflects food habits which prey groups (e.g. zooplanktivorous include prey from freshwater and terres­ Alcidae). Additionally, due to the dilu­ trial environments. Thus although diver­ tion effect of the marine environment, sity appears to be great for digeneans in the probability of establishing infections some avian taxa, the values are inflated in suitable intermediate hosts would be with respect to single records of other­ reduced in oceanic regimes. Faunas wise incidental parasites, and those typical of oceanic islands appear to be which are not derived from marine reduced in contrast to those associated communities. with continental islands where foraging Ecological relationships of hosts are opportunities and potential prey sources of primary importance in determining the for marine birds may be of greater diver­ distribution of digcncans. The occur­ sity. rence of flukes will he influenced by Digeneans should as a consequence food habits and foraging patterns, and be limited in distribution by a range of diversity may be related to the variety of factors related to focality. These include: prey species selected by the final host 1) first intermediate hosts are mollusks; (Kennedy et a/, 19R6; but see Poulin, 2) the dispersal stage, the cercaria, 1995, 1996). In insular marine systems possesses potentially limited capabilities there arc additional limitations inherent for long-term survival in the plankton in life cycles which will further tend to prior to encountering a second interme­ influence the occurrence of digeneans, diate or final host (schistosomes); and 3) and account for their absence in oceanic second intermediate hosts may be rela­ seabirds (Table 11). tively sessile demersal fishes or benthic Ultimately transmission is dependent invertebrates with limited abilities for on the distri bution of intermediate hosts dispersal (e.g. Araki & Machida, 1990; (invertebrate and vertebrate prey spe­ Tsimbaliuk et al, 1968). Thus, cycles cies) and their availabi lity to the final will be limited to a species assemblage host. In this regard, an oceanic island can inhabiting a well defined geographic region, potentially resulting in some 74 degree of endemism for parasites. Pat­ Helminths as contemporary biodiver­ terns will be further influenced by sea­ sity probes: sonal, behavioral and other ecological Parasitic helminths are exquisite determinants (Bartoli, 1989). ecological indicators because their Abiotic controls on transmission also complex life cycles are tied to intricate may be evident for digeneans and other food webs where a series of intermediate helminths. Oceanographic fronts and and paratenic hosts are necessary for tidal eddy systems adjacent to islands successful parasite transmission. Para­ concentrate prey utilized by seabirds and sites track broadly and predictably marine mammals (Hunt & Schneider, across many trophic levels. Thus, the 1987; Hunt et al, 1988; Wolanski & occurrence and abundance of digeneans Hamner, 1988). Predictable and persis­ and other helminths can be applied in an tent zones of circulation associated with hierarchical manner to explore a range of insular and pelagic systems should trophic and ecological associations (see represent foci for parasite transmission Bartoli, 1989; Hoberg, 1992a). Where (Hoberg, 1986a, 1995). Mixed-species life cycles, along with ancillary aspects assemblages of seabirds attracted to of transmission related to biological, zones of upwelling and convergence seasonal and environmental controls are often exploit a narrow spectrum of understood, helminths become powerful macrozooplankton and nekton. These ecological probes (Bartoli, 1989). circumstances could enhance the main­ Guilds, involving phylogenetically tenance of parasite-host assemblages in disparate seabirds (and other vertebrates) regions where seabirds and potential exploiting common prey resources, are intermediate hosts would be concen­ the highest level of trophic interactions trated for extended periods of times. which can be evaluated using helminths Parasitological data and a biodiversity (e.g. Hoberg, 1983). Belogurov (1966) research program: examined the interactions among orders of avian hosts and among avian and Although a small percentage of mammalian hosts on coastal areas of the species of helminths from seabirds have Sea of Okhotsk. In this instance overlap so far been described, a considerable in food habits, foraging behavior and use body of information is available on life of habitat among charadriiforms, pele­ history and distribution which can be caniforms, and anseriforms was indi­ applied in ecological and historical cated by a diversity of platyhelminths, assessments of biotas. Historically, such nematodes and acanthocephalans, shared data have been of intrinsic importance among host-groups. Guild associations only to parasitologists. However, it is are significant in driving the potential becoming recognized in the zoological for colonization or host switching by community that these data can directly parasites among ecologically similar complement and augment knowledge vertebrates (Bush et al, 1990; Hoberg, derived solely from the study of free­ 1987b). living organisms on which parasites are dependent and thus are of integral im­ Comparisons between distinct feed­ portance in biodiversity research (Brooks ing guilds are also instructive with et al, 1992; Hoberg, 1996). respect to the influences on the distribu- 75 tion of helminths. In the North Pacific, parasites were acquired from marine zooplanktivores (species of auklets, (Aporchis massiliensis Timon-David, Aethia Merrem, C. psittacula) support a 1955), brackish (C. longicollis), fresh­ fauna which is distinct from that of larids water (Diplostomum spathacaeum and other alcids particularly murres (Rudolphi, 1819) or terrestrial (Brachy­ (Uria lomiva (Linnaeus), U. aalge laima fuscatum (Rudolphi, 1819)) envi­ (Pontoppidan)), guillemots, (species of ronments. The principles are broadly Cepphus Pallas) and puffins (species of applicable and are illustrated by the Fratercula Brisson and Cerorhinca following examples from the North moncerata (Pallas)) (Hoberg, 1984a, Pacific basin and Antarctica. 1992a). This may be a fu nction of zona­ Prevalence of cestodes can be indica­ tion in foraging (distance from islands tive of dietary differences. Variation in and depth) (Bedard, 1976; V ermeer et al, the occurrence of A. armillaris between 1987), vertical zonal ion of macrozoo­ the congeners of murres appears to plankton and nekton and their availabil­ reflect segregation in diets. At mega­ ity as prey (e.g. via die! migrations), and colonies in the Holarctic where both differences in body-size and feeding species of murres have been examined, capability of potential intermediate hosts A. armillaris was generally more com­ I (see I-Ioberg, 9�4a). In the western mon in thick-billed murres (reviewed in Antarctic, segrcgat ion in foraging was I-Ioberg, 1984a). Euphausiids are known demonstrated by the limited distribution intermediate hosts for some species of of acanthoccphalans, digencans, and by Alcataenia (see Shimazu, 1975). Thus, distinct cestode faunas in gu lls. (I-Ioberg, substantial differences in prevalence of 1983, 1984b, I <)�6h; Hoberg unpub­ A. armillaris are indicative of dissimi­ lished data). However, the distribution of larity in the diets of murres, as macro­ Te trabothrius among penguins, procel­ zooplankton are of greater importance lariiforms, and shags, is also highly for U. lamvia (Hunt et al, 1981). segregated but has a phyloge­ netic/historical basis (Baer, 1954; Levels of parasitism between horned Hoberg, 19�7a). (Fratercula corniculata) and tufted puffins (F. cirrhata) can also be partially In a more refined manner, helminths explained by differences in prey selec­ are useful as direct indicators of host­ tion (see Hoberg, 1984a, 1992a). Horned diet, including aspects of prey selection puffins consume greater numbers of among species, or het ween sexes and age invetiebrates and forage closer to shore classes among conspecifics. Bartoli than tufted puffins (Ainley & Sanger, (1989) showed that certain digenetic 1979; Hunt et al, 1981; Wehle, 1983). trematodes, bccausL� of their life histories This is reflected in the distribution of and dependence on specific intermediate anisakine nematodes (species of Contra­ hosts, could be used to indicate host-diet caecum Railliet and Henry, 1912) which in yellow-legged gulls. Based on compo­ are significantly more abundant in F. nents of the digenean fauna, it was cirrhata. For instance at Buldir Island, possible to identify particular fishes (e.g. Aleutian Islands and at Talan Island, Sea Cardiocephalus longicollis (Rudolphi, of Okhotsk, tufted puffins were consis­ 1819)), mollusks (Gymnophallus delicio­ tently more heavily infected (99% of 99 sus (Olsson, 1893)), and crustaceans and 83% of 30) than horned puffins (Megalophallus carcini (Prevot and (50% of 77 and 13% of 30) (Hoberg, Deblock, I 970)) as prey and whether 76

I 984a; I 992a; Hoberg unpublished alcids and larids in the North Pacific data). This constitutes a trend at other (Hatch et al., 1993; Hunt et al., 1981; sites in the western Bering Sea and Sea Vermeer et al, 1987). In this regard the of Okhotsk (Belogurov et al, I 968; very high prevalence of A. armillaris Tsimbaliuk & Belogurov, I964). How­ (84%) among thick-billed murres at St. ever the substantial differences in the Matthew Island, Bering Sea, coincided cestode faunas between these congeners with a breeding failure at that site in is considered to have a phylogenetic 1982 (Hoberg, 1984a). Reproductive basis (Hoberg, 1986a, 1992b; Hoberg et success was reduced presumably be­ al, I 996). cause adequate numbers of fish were not Distinct segregation in food-habits available for adults to bring to chicks also may be demonstrated between adult, (see Springer et al, 1986). nestling and fledgling conspecifics. Overall helminth diversity (compo­ Among large gulls and medium to large nent generic and species-richness; see alcids, helminths indicate that nestlings Bush et al, 1990) and the occurrence of receive a minimal component of crusta­ unique parasites can indicate habitat and ceans from adult birds. For example, at foraging distributions for birds. Distinct Talan Island, species of Alcataenia were differences were noted when birds absent or only occurred sporadically in foraging predominately in littoral zones fledgling kittiwakes (Rissa tridactyla are compared to those which disperse (Linnaeus)) (8% of 26), and horned from colony sites over the continental puffins (0 of 28), but were dominant in shelf and oceanic waters. This is a adult birds (63% of 30; 47% of 30). general trend among alcids, larids and Conversely, among fledgling kittiwakes procellariids in the Northern Hemisphere the prevalence of Te trabothrius (96%) and among penguins, procellariiforms and Contracaecum (54%) was substan­ and larids in the Antarctic. Species tially greater than in breeding birds (20% richness of the helminth faunas of pe­ and 0). Contracaecum was also more lagic foragers is generally substantially common in fledglings of horned puffins lower than that observed in birds which (64% versus 13%). These trends were feed adjacent to colony sites (Hoberg, also evident, but not as clearly defined 1984a, 1984b, 1986b, 1992a; Hoberg & among murres and slaty-backed gulls Ryan, I 989; Hoberg unpublished data). (Larus schistisagus Stej neger), sympa­ A classic comparison involves adults tric at this colony. Piscine paratenic of Larus spp. and black-legged kitti­ hosts are important in transmission of wakes in the North Pacific basin. The Contracaecum, and have been postulated helminth faunas of kittiwakes are most as intermediate or paratenic hosts for similar to those characterisitc of pelagic some species of Tetrabothrius (Hoberg, birds rather than other larids. Kittiwakes 1987b). Overall the distribution of cesto­ are the most pelagic of the gulls (Hatch des, digeneans and nematodes found in et al, I993; Vermeer et al, I993b) and alcids and larids at this colony indicated across the Holarctic generic-level rich­ that adult birds foraged on an array of ness of gastrointestinal faunas is low ( 4- mollusks, crustaceans, and fishes, while 8 at any specific colony site) (Hoberg, preferentially providing piscine prey to I 992a; Hoberg, unpublished data). These rapidly developing chicks (Hoberg, values are similar to those for a range of I 992a). This is consistent with observa­ species of alcids (0-8 genera of he!- tions on food-habits established for 77

minths) at sites across the North Pacific (Linnaeus)) in northern latitudes, nor are basin (Hoberg, unpublished data). In parasites apparently acquired during contrast, species of gulls (in this case migration. Larus schistisagus or Larus glaucescens Within an extensive geographic zone, Naumann) which forage in the littoral parasites can be applied to elucidation of zone and a wider range of environments patterns of migration or dispersal. Bar­ supported in excess of 20 genera at some toli (1989) showed that the digenean, localities (range 13 - >20). The only Gymnophallus deliciosus, in yellow­ exception to this across the Holarctic legged gulls collected at Corsica was was observed in a colony of kittiwakes at acquired by birds resident along the Talan Island. At this location, 12 genera northern European coast, thus confirm­ were reported from adult birds. This ing the migratory path for this !arid. On a level of diversity far exceeded that broader scale the distribution of kidney observed ( 4-6) at any site in the North flukes (species of Renicola Cohn, 1904), Pacific and Bering Sea. The occurrence may be useful for identification of birds of trematodes, and the great abundance which have dispersed in the North Pa­ of Cryptocotyle lingua (Creplin, 1825), cific basin. Species of Renicola are indicated that kittiwakes at Talan Island characteristic of phalacrocoracids, larids, foraged to a greater extent in nearshore and alcids in the Sea of Okhotsk and Sea habitats and exploited a wide variety of of Japan, but appear to be virtually molluscan and piscine prey. Higher absent in these marine birds from the levels of generic diversity appear con­ Aleutian Islands, Gulf of Alaska and sistent for the Okhotsk Sea (Belogurov et Bering Sea and the eastern North Pacific al, 1968). This exception is notable as it (Hoberg, 1984a, 1992a). This apparent may signify fundamental diffe rences in endemism for species of Renicola in the how communities of marine birds func­ western Bering Sea, Sea of Okhotsk and tion in distinct regions of the North Sea of Japan (Belogurov et a!, 1968; Pacific basin. Leonov et al, 1965) would support use Parasitic helminths and geographic of these trematodes as biological indi­ distribution: cators for the origin of some avian species. Parasites allow recognition of the origin of birds, with respect to breeding Parasites as historical biodiversity grounds, or residence in a geographic probes: region (Dogiel, 1964). Helminth faunas There are ecological and geographic of shearwaters (species of Puffinus factors which influence the distribution Brisson, Proccllariiformcs) which mi­ of helminths. Additionally, faunas are grate into the Northern Hemisphere structured by historical/phylogenetic during the boreal summer are largely effects which result in characteristic distinct from those typical of procellarii­ patterns of host-association and bio­ forms and other seabirds in the Holarctic geography (Brooks & McLennan, 1991; (Hoberg & Ryan, I 989; Hoberg, unpub­ 1993). These patterns are linked to pro­ lished data; et al, I 996). Cestodes, cesses through evaluation of alternative, and trematodes acquired on southern but not mutually exclusive hypotheses breeding colonies arc not exchanged for cospeciation or colonization (host­ with a fauna associated with procellari­ switching) (Brooks & McLennan, 1991, ids, such as fulmars (Fulmarus glacialis 78

1993; Hoberg, 1 992b, 1996; Hoberg et Alcataenia and the tetrabothriids are al, 1996). briefly examined below, and form the An early example of application of conceptual basis for development of an these principles was the proposal by historical research program for Szidat (1964) for affinity between south­ helminths of marine birds. ern black-backed gulls (Larus dominica­ The tetrabothriids present a compli­ nus Lichtenstein) of the Antarctic and cated and archaic history associated with the assemblage including Larus marinus seabirds, extending at a minimum to the Linnaeus in the North Atlantic (Hoberg, early Tertiary. The origin of the group is 1986c; Stadler, 1975). The putative attributable to colonization of marine relationship was based on the concept of birds or mammals by tetraphyllidean cospeciation, where both gulls and cestodes of chondrichthians (Galkin, parasites shared common ancestors prior 1987; Hoberg, 1987b; Hoberg & Adams, to isolation and divergence in the North­ 1992). Remarkably, a dominant group of ern and Southern Hemispheres (Hoberg, cestodes among seabirds radiated fol­ 1986c). Since then, a robust methodol­ lowing a host-switch from marine fishes ogy has been developed to formulate and to homeotherms. This reinforces the evaluate hypotheses for cospeciation and importance of guild associations, and historical biogeography (Brooks, 1981; evolutionary time in the development of Brooks & McLennan, 1991, 1993; biotas. Hoberg et al, 1996; Page, 1993). How­ Seabirds are considered to represent ever, among seabirds and avian host­ the basal or ancestral hosts for parasite systems in general there have tetrabothriids, and species-groups of been few studies addressing these issues Tetrabothrius (and Chaetophallus in with respect to helminth parasites procellariiforms) constitute core faunas (Hoberg, 1996; Hoberg et al, 1996). among each of the 6 orders of seabirds Historical studies to date among seabirds (Baer, 1954; Temirova and Skriabin, have been limited to tapeworm faunas of 1978; Hoberg, 1987a; 1987b; Hoberg & the Alcidae (Hoberg 1986a, 1992b) and Adams, 1992). Species are generally the Podicipediformes (Stock, 1985). host-specific at the level of avian order, Preliminary studies have been conducted potentially implying long-term coevolu­ among the tetrabothriids, the dominant tionary associations (but see Hoberg, group of cestodes among seabirds 1986a; Hoberg et al, 1996, for excep­ (Hoberg, 1987a; 1987b; Hoberg & tions). Although phylogenetic analyses Adams, 1992). are required to reconstruct the host and Historical studies of helminths among biogeographic histories for these cesto­ vertebrates have shown that cospeciation des (e.g. Brooks & McLennan, 1991), is not a universal phenomenon (Brooks certain aspects of their host associations & McLennan, 1993; Hoberg et al, 1996). suggest that they represent an archaic Patterns of archaic cospeciation (Podici­ fauna. pediformes and cestodes), archaic colo­ The phylogeny of marine birds is nization and secondary radiation (Tetra­ complex and has yet to be adequately bothriidae) and recent colonization and resolved (see Cracraft, 1985; Hedges & diversification in a restricted group of Sibley, 1 994). With respect to hosts for hosts (Alcidae and Alcataenia) have Te trabothrius, an emerging consensus been recognized. The relationships for for relationships can be recognized: 1) a 79

Podicipediformes [!]

[!]

Phalacrocoracidae � � �

"Ciconiiformes" �

� �

�

• 42 spp. of totrabothriids � • Host .. spocific at "ordinal" level • 1 sp. sharod amonp orders [I]

[I]

Figure l. Phylogenctic relationships for orders of marine birds (modified from Hedges & Sibley, 1994 ), with numbers of tetrabothriids (in boxes) mapped onto the host tree showing distribution of diversity. Tl!e relative relationships of the 6 "orders" of marine birds are shown within the context of a larger avian phylogeny. Note the following: 1) polyphyly for the "Pelecaniformes", indicated by placement of the Phaethontidae, Pelecanidae, and Fregatidae relative to classical pelccaniforms (see Cracraft, 1985); 2) the affinities of the Fregatidae, penguins, loons, and tube-noses; and 3) independence of the Charadriiformes (in separate box). A putative relationship with the "Ciconiiformes" suggests that the marine environment was colonized independently by diffe rent avian taxa. There are 42 species of Te trabothrius and Chaetopha/lus in seabirds. All are host-specific except, T pelecani Rudolphi, 1819 is shared between sulids and fregatids, and T. macrocephalus (Rudolphi, 1810) occurs in Charadriifor­ mes, Gaviiformes, Podicipccliformes and Pelecaniformes, and incidentally in Anseriformes (Temirova & SkJjabin, 1978). 80 close affinity for the penguins, procel­ The specific distribution of Tetra­ lariiforms and possibly gaviiforms; 2) bothrius spp. among shags (Leuco­ polyphyly for the pelecaniforms; and 3) carboninae, Phalacrocoracidae) further charadriiforms are not closely related to suggests archaic associations (Hoberg, this assemblage. Thus, if the distribution 1987a). Among phalacrocoracids, only of species of Te trabothrius is mapped Notocarbo bransfieldensis (Murphy) onto the putative host phylogeny (Fig. (with T. shinni Hoberg, 1987) in western 1), patterns of both colonization and Antarctica and Stictocarbo aristotellis cospeciation are apparent. If cospecia­ (Linnaeus) (with T. phalacrocoracis tion has been a dominant mechanism in Burt, 1977) in the North Atlantic are diversification, then those cestodes in the known hosts; an additional species may Fregatidae + Sphenisciformes + Gavii­ occur in S. urile (Gmelin) in the Aleutian formes + Procellariiformes, those in Islands (Hoberg unpublished data). Charadriiformes and those in "Pelecani­ These are morphologically similar formes" may represent monophyletic species of parasites, with highly disjunct assemblages related at some basal level. ranges, occurring in phylogenetically By necessity this implies multiple colo­ related hosts in the Northern and South­ nization events, associated with inde­ ern Hemispheres. Such observations, in pendent acquisition of marine life histo­ conjunction with the biogeography of ries by different groups of birds, with the the host group (Siegei-Causey, 1988; potential for cospeciation being dictated 1992), are consistent with an hypothesis by the timing of the host switch. for initial diversification of this assem-

Figure 2. Phylogenetic relationships for the "pelecaniform" birds (modified from Hedges & Sibley, 1994 ), with the distribution Te trabothrius spp. (numbers in boxes) mapped onto the host tree. This tree is consistent with polyphyly, with the pelecanids and fregatids being more closely related to other avian groups (denoted by independant boxes). The distribution of cestodes suggests historical-ecological constraints on host association, with obligate marine life cycles. This accounts for absence of species in anhingas and occurrence only in marine pha­ lacrocoracids, sulids and phaethontids. 81

blage in the Southern Ocean during the fins, mmTes, guillemots, and some early Tertiary. auklets) and Laridae yielded a general Additionally, the distribution of area relationship or pattern for host and Tetrabothrius spp. in "pelecaniforms" parasite diversification in the North indicates that parasites were lost in hosts Pacific basin, North Atlantic, and ad­ that secondarily reinvaded freshwater joining areas of the Arctic (Fig. 3) (Ho­ systems (Fig. 2). This further accounts berg, 1992b; Hoberg et al, 1996). Radia­ for absence of these cestodes in anhingas tion for hosts and parasites during the and their sporadic occurrence among the late Pliocene and Pleistocene was linked phalacrocoracids. to climatic factors (glaciations) driving cyclical fluctuations in sealevel and Tetrabothriids among seabirds repre­ environmental disruption (Hoberg, sent a robust model system for examin­ 1986a, 1995). In this regime, there were ing the roles of historical ecological alternating periods of geographic isola­ interactions and cospeciation in diversi­ tion and range expansion from refugial fication. What remains to be addressed is habitats along marginal zones of the the 1) phylogeny of Tetrahothrius spp. to North Pacific, Sea of Okhotsk, Aleutian indicate whether core faunas are mono­ Islands, and Arctic basin. As a conse­ phyletic; 2) potential timing of coloniza­ quence, this fauna was structured pri­ tion for orders, based on cospeciation marily by host-switching and geographi­ analysis (Hoberg et al., 1996); 3) the cal colonization over the past 3 million history of subsequent diversification; years, a pattern congruent with that whether this has been via colonization or postulated for cestodes among phocine some level of cospeciation; and 4) his­ pinnipeds (Hoberg, 1992b, 1995; Hoberg torical biogeography and historical & Adams, 1992). In this instance, the ecology (Brooks & McLennan, 1991). assemblage of Alcataenia-Alcidae re­ The history of the tetrabothriids is one of flects specific ecological linkages via the major unresolved enigmas for evolu­ food webs that have been maintained tion of cestode faunas (Baer, 1954; since at least the late Pliocene. These Galkin, 1987; Iloberg, 1987b). studies constituted the foundation for the Historical research using host- Arctic Refugium Hypothesis which parasite phylogeny has involved faunas provides the conceptual basis for under­ with relatively ancient origins and the standing historical biogeography of the tetrabothriids appear in this category North Pacific and Arctic basin since the (Hoberg, 1996). It is also possible to Pliocene (Hoberg, 1986a, 1992b, 1995; examine associations that have relatively Hoberg & Adams, 1992). recent derivations. For example, consider Seabird helminths and marine biodi­ the patterns of distribution and specia­ versity - a developing research pro­ tion that have been postulated for Al­ gram: cataenia and the Alcidae and their application to elucidation of bin­ Future studies of parasite faunas geographic processes across the Holarc­ among marine birds should concentrate tic (Hoberg, 1986a, 1992b, 1995; Hoberg in a variety of areas. Survey and inven­ & Adams, 1992; Hoberg et al, 1996). tory remains requisite in establishing Phylogenetic and historical bin­ baselines for poorly studied avian taxa, geographic analyses of these cestodes communities and regions. Although the among the Alcidae (principally in puf- procellariiforms are among the most 82

.;' / / / I I I I I I I I I I I I FR I I I I LA \ I \ I \ I \ I \ I \ I \ I \ I \ I \ I \ I ' I ' I ' ' / ' / ' / ' / / / / /

Figure 3. Area relationships for species of Alcataenia, a host specific group of cestodes among the Alcidae (modified from Hoberg, I 992b) . The phylogenetic tree fo r 9 species of Alcataenia is superimposed over the geographic range for the host and parasite group in the Holarctic. Two primary areas of diversity are recognized: (I) a putative ancestral area in the North Atlantic sector of the Arctic basin that is consistent with a Holarctic distribution for the basal species A. larina (LA) (in larids); and (2) a region of secondary diversification for A. fraterculae (FR) (horned puffins), A. cerorhincae (CE) (rhinoceros auklets), A. pygmaeus (PY) (whiskered auklets), A. armillaris (AR) (murres), A. longicervica (LO) (murres), A. mei­ nertzhageni (ME) (murres), and A. campylacantha (CA) (guillemots) in the North Pacific. This general pattern resulted from early vicariance of a Holarctic fauna across the Beringian region, followed by radiation in the North Pacific with subsequent range expansion into the Arctic basin and Atlantic for murres, guillemots and their tapeworms. Changes in sealevel as an influence on distribution is indicated by the extent of exposed continental shelf during glacial maxima (stippled regions, modified from Wise & Schopf, 1981 ) . The map shows the limits of the geographic range for Alcataenia (dashed lines across the North Pacific and North Atlantic). 83 poorly known, significant work remains distribution of seabirds (Ainley & Boek­ to be conducted within most orders. It is elheide, 1990). Changes in circulation, imperative from a scientific and ethical upwelling regimes, and water masses are basis that parasitology be integrated with reflected in food web structure ongoing ornithological research, par­ (distribution of primary production, ticularly within the arena of collections­ �ooplan�ton and fishes) and ultimately based investigations for trophic ecology, m parasite faunas. Parasites should be biogeography and systematics. There is a admirably suited to tracking cyclical necessity to derive the maximum level of variation in trophic dynamics and distri­ information from any scientific collec­ bution of seabirds. tions. The helminth faunas of seabirds have Although much remains to be learned been structured by historical and eco­ about the diversity of helminths among logical determinants. It is evident that marine birds, it is clear that parasites parasites are useful in mapping variation constitute significant probes for biodi­ in fauna! diversity over temporal scales versity research. The utility of an histori­ ranging from a few years to the millen­ cal research program for hosts and nia of evolutionary time. As a conse­ parasites is indicated by the substantial quence parasites constitute powerful insights that can be gained about marine tools to be applied to questions about the communities over evolutionari ly signifi­ origin, maintenance and distribution of cant time frames. As historical probes, organismal diversity in marine commu­ parasites are critical to examinations of nities. biogeography and ecology and in eluci­ Acknowledgements dating the development of biotas and Research discussed in this review regions. The complex life histories of was supported over many years by a parasites, dependent on the temporal diversity of sources: in Antarctica by the continuity of ecological linkages in a National Science Foundation DPP- community, become keys for under­ 8115975; in the North Pacific and Chuk­ standing the historical formation of hotka by the Arctic Institute of North biotas. The methodological framework America, and the National Academy of now exists for rapid advances in this Sciences Interacademy Exchange Pro­ research program, however there contin­ gram; in Russia, by the Russian Acad­ ues to be a paucity of phylogenetic emy of Sciences and the Laboratories of hypotheses for hosts and parasites, and a Parasitology and Ornithology of the dearth of systemtists dedicated to most Institute of Biological Problems of the organismal groups (Hoberg et al, 1996). North, Magadan. Field work in Alaska At a contemporary level, a predictive was made possible by the US Fish and foundation can be developed from on­ Wildlife Service. Russian colleagues, going efforts in biodiversity assessment. particularly Alexander Kondratiev, The predictive power of parasitology Svetlana Bondarenko and Alexander becomes of increasing importance when Kitayski contributed significantly to attempts are made to elucidate impacts success of field work on Talan Island. from natural or anthropogenic perturba­ Other collections, supported by Garret tions to faunas and ecosystems. Consider Eddy, were conducted in conjunction the effect of the El Nifio-Southern Os­ with Sievert Rohwer and colleagues cillation on reproductive success and from the Thomas Burke Memorial 84

Washington State Museum, University Monbailliu X, and Paterson AM, eds. Status of Washington. Robert Storer kindly and conservation of seabirds ecogeography made available summary statistics for and Mediterranean action plan. Madrid: parasite faunas in grebes. I thank Marga­ Society of Spanish Ornithology, 1989: 25 1-9 ret Dykes-Hoberg for preparation of the Bartonek JC, Nettleship DN, eds. Conserva­ cladograms. Also, appreciation is ex­ tion of marine birds of northern North tended to Ann Adams and Douglas America. Washington, DC: United states Siegel-Causey for their insightful and Department of the Interior, Fish and Wildlife critical reviews. Service, 1979 Barus V, Sergeeva TP, Sonin MD, Ryzhikov References KM. Helminths of fish-eating birds of the Ainley DG, Boekelheide RJ, eds. Seabirds of Palearctic region I. The Hague: W. Junk the Farallon Islands, ecology, dynamics, and Publishers, 1978 structure of an upwelling-system community. Bedard J. Coexistence, coevolution and Stanford: Stanford University Press, 1 990 convergent evolution in seabird communities: Ainley DG, Sanger GA. Trophic relations of a comment. Ecology 1976; 57: 177-84 seabirds in the northwestern Pacific Ocean Belogurov OI. Spetsifichnost' gel'mintov v and Bering Sea. In: Bartonek JC and Nettle­ otnoshenii definitivnykh khoziaev vzai­ ship D, eds. Conservation of marine birds of mosiaz' gel'mintofauna zhivotnykh razlich­ northern North America. Washington DC: nykh otriadov. Zoo! Zhurnal 1966; 45: 1449- US fish and Wildlife Service, Report No. 11, 54 1979: 95-122 Belogurov OI, Leonov VA, Zueva LS. Lilli­ Araki J, Machida M. Metacercariae of Gel'mintofauna ryboiadnykh ptits (chaek i atrema sobolevi Hexagram­ from greenling chistikov) poberezh'ia okhotskogo moria. In: mos agrammus. Jpn J Parasitol 1990; 39: Gel'minty zhivotnykh tikhogo okeana. 63 1-3 Moskva: Izdatl'stvo Akademii Nauk SSSR, Ashmole NP. Seabird ecology and the marine 1968: 105-24 environment. In: Farner DS, King JR, and Belopol'skaya MM. Parazitofauna morskikh Parks KC, eds. Avian Biology. New York: vodoplavaiushchikh ptits. Leningrad Univer­ Academic Press, 1971: 223-86 sitet Uchenye Zapiski, Seriia Biologicheskikh Baer JG. Revision taxonomique et etude Nauk 1952; 141: 129-80 biologique des cestodes de la famille des Belopol'skii LO. The ecology of sea colony Tetrabothriidae parasites d'oiseaux de haute birds of the Barents Sea. Moskva: mer et de mammireres marins. Memoires de Izdatel'stvo Akademii Nauk SSSR, 1957. l'Universite de Neuchatel 1954; 1: 4-122 [English Translation, Jerusalem: Israel Baird W. Descriptions of some new species Program for Scientific Translations, 1961] of Entozoa from the collections of the British Bondarenko SK. Ramitserk v zhiznennykh Museum. Proc Zoo! Soc 1853; 18-25 tsiklakh trekh vidov roda Aploparaksis Bakke TA. Checklist of helminth parasites of (Cestoda) parazitov kulikov. Parazitologiia the common gull (Larus canus L.). Rhi­ 1993; 27 : 375-86 zocrinus 1972; 1: 1-20 Bondarenko SK, Kondrat'eva LF, Khoberg Bakke TA. Studies of the helminth fauna of EP. Parazit chaek Hymenolepis (s.l.) halde­ Norway XL: The common gull, Larus canus mani Schiller, 1951 i ego zhiznennyii tsikl. L., as final host for Cestoda (Platyhel­ Acta Parasitol Lithuan 1987; 22: 82-91 minthes). Fauna Norv 1985; 6: 42-54 Bourgeois CE, Threlfall W. Parasites of the Bartoli P. Digenetic trematodes as bio­ greater shearwater (Puffinus gravis) from indicators for yellow-legged gulls in Corsica Newfoundland, Canada. Can J Zoo! 1979; (Western Mediterranean). In: Aguilar JS, 1355-7 85

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Shuntov VP. Seabirds and the biological Albans: Technical Communication 37, Com­ structure of the ocean. Vladivostok: monwealth Bureau of Helminthology, 1966 Dal'nevostochnoe Knizhnoe Izdatel'stvo, Threlfall W. Studies on the helminth para­ 1972. [English Translation, Bureau of Sport sites if the herring gull, Larus argentatus Fisheries and Wildlife, 1974) Pontopp., in Northern Caernarvonshire and Smetanina ZB. Gel'minty morskikh ryboiad­ Anglesey. Parasitology 1967; 57: 43 1 -53 nykh ptits Zaleva Petra Velikovo. Vladivos­ Threlfall W. The helminth parasites of three tok: Biologiia i sistematika gel'mintov zhiv­ species of gulls in Newfoundland. Can J Zoo! otnykh Dal'nego Vostoka, 1981: 71-81 1968; 46: 827-30 Smetanina ZB , Leonov VA. Gel'minty Threlfall W. Helminth parasites of alcids in ryboiadnykh ptits Kyril'skikh ostrovov. In: the northwestern North Atlantic. Can J Zoo! Biologiia i taksonomiia gel'mintov zhivot­ 1971: 461-6 nykh i cheloveka. Moskva: Akademiia Nauk SSSR, 1984: 59-66 Torres P, Ruiz E, Gesche W, Montefusco A. Gastrointestinal helminths of fish-eating birds Springer AM, Roseneau DG, Lloyd DS, fi·om Chiloe Island, Chile. H. Wldlf Dis McRoy CP, Murphy EC. Seabird responses 1991; 27: 178-9 to fluctuating prey availability in the eastern Bering Sea. Mar Ecol Prog Ser 1986; 32: 1- Tsimbaliuk AK, Belogurov 01. 0 faune 12 nematod ryboiadnykh ptits ostrovov berin­ gova moria. Nauchnoi Doklady Vyssheii Spasskaya LP. Tsestody ptits SSSR, gime­ Shkoly Biologicheskie Nauki 1964; 4: 7- 11 nolepididy. Moskva: Akademiia Nauk Moldavskoi SSR Insitut Zoologii, Izdatel'stvo Tsimbaliuk AK, Kulikov VV, Bm·anova TI, Nauka, 1966 Tsimbaliuk EM. Bespovonochnye litorali ostrova Beringapromezhutochnye i dopol­ Spasskii AA. Osnovy tsestodologii II. Gime­ nitel'nye khoziaeva gel'mintov ptits i nolepididy Ientochnye gel'minty dikikh i mlekopitaiushchikh. Yladivostok: Gel'minty domashnikh ptits. Moskva: Izdatel'stvo zhivotnykh Tikogo Okeana, Izdatel'stvo Akademii Nauk SSSR, 1963 Nauka 1968, 129-52 Stadler T. Clave para un problema. Antartida Yermeer K, Briggs KT, Mm·gan KH, Siegel­ 1975; 6: 48-9 Causey D, eels. The status, ecology and Szidat L. Vergleichende helminthologische conservation of marine birds of the North Untersuchungen an den argentinischen Pacific. Ottawa: Canadian Wildlife Service, Grossmowen Larus marinus dominicanus 1993a Larus ridibundus maculi­ Lichtenstein und Vermeer K, Irons DB, Velarde E, Watanuki pennis Lichtenstein nebst neuen Beobachtun­ Y. Status, conservation and management of gen iiber die Artbildung bei Parasiten. Z f nesting Larus gulls in the North Pacific. In: Parasitenkd 1964; 24: 351-4 I 4 Yermeer K, Briggs KT, Morgan KH, and Stock TM. Patterns of community ecology Siegel-Causey D, eels. The status, ecology and coevolution of intestinal helminths in and conservation of marine birds of the North grebes. Doctoral Dissertation, Edmonton: Pacific. Ottawa: Canadian Wildlife Service University of Alberta, 1985 Special Publication, 1993b: 131-9 Temirova SI, Skrj abin AS. Tetrabotriaty i Yermeer K, Sealy SG, Sanger GA. Feeding mezotsestoidaty lentochnye gel'minty ptits i ecology of Alcidae in the eastern North mlekopitaiushchikh. Osnovy Tsestodologii 9. Pacific Ocean. In: Croxall JP, eel. Seabirds: Moskva: Izdatel'stvo Nauka, Akademiia feeding ecology and role in marine ecosys­ Nauka SSSR, 1978 tems. Cambridge: Cambridge University Threlfall W. The helminth parasites of the Press, 1987: 187-227 herring gull (Larus argentatus Pontopp.). St. 89

Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH. Sampling effort and para­ site species richness. Parasitol Today 1995; 11: 306- 1 () Wehle, DSH. The food, feeding and devel­ opment of young tufted puffins in Alaska. Condor 1983; 85: 427-42 Williams IC, Jones NV, Payne MJ, Ellis C. The helminth parasites of the sheathbill, Chionis alba (Gmelin), and the diving petrels, Pelecanoides f.ieorf.iicus (Murphy and Harper) and P. urinatrix (Gmelin) at Bird Island South Georgia. J 1-Ielminthol 1974; 48: 195-7 Wise KP, Sehopf TJ M. Was marine fauna! diversity in the l'leistocene affected by changes in sea level? Paleobiol 1981; 7: 394- 9 Wolanski E, Hamner WM. 1988. Topog­ raphically controlled fronts in the ocean and their biological influence. Science 1988; 241: 177-81 Yamaguti S. Synopsis of digenetic trema­ todes. Tokyo: Keigaku, I 97 I Zdzitowieeki K. Acanthoccphalans of birds from South Shetlands (Antarctic). Acta Parasitol Polon l 9X:i;30: 11-24 Zdzitowieeki K, Szelcnbaum-Cielecka D. Anomotaenia dominicanrJ (Railliet et Henry, 1912) (Cestoda: Dilepididac) from the Dominican gull IAI!"Ils dominicanus Licht. of the Antarctic. Acta l'arasitol l'ol

THE COMMON EIDER - SOME ECOLOGICAL AND ECONOMICAL ASPECTS

Kristinn H. Skarphedinsson Icelandic Institute of Natural History, Hlemmur 3, 105 Reykjavik, Iceland

Abstract

The common eider Somateria mollis­ today, little down is harvested, except in sima is locally important economically Iceland where eider down harvest is and one of the best studied birds of locally important and 3,000 kg of down northern latitudes. The potentially high are marketed annually. Current eider reproductive output is compensated by husbandry practices in Iceland, which variable, but usually high duckling appear to be extremely effective in mortality. Adult survival rates are high maintaining a high nest success (over and typical of a seabird. Long term 80%), are discussed at length. population changes are poorly under­ Managing eiders for down harvest stood, except in areas where over­ should focus on improving adult survival harvesting constitutes a serious problem. rates and nest success. As many hunted Most eider populations are shared by eider populations are over-harvested, the more than one country, hence eider con­ emphasis should be placed on reducing servation depends on international co­ hunting related mortalities, either by operation and agreements. Population protecting eiders or by strict bag limits. trends are in part explained by different Introduction: management strategies. Increased pro­ tection offered to some populations The common eider is locally impor­ seems to have resulted in general impro­ tant economically and one of the best vement of their status. On the other hand studied birds of northern latitudes. over-harvesting is apparently responsible Thousands of research papers have dealt for the reduction in other eider populati­ with various aspects of eider biology. ons. Most of the studies have been conducted in eastern North America and northern Eiders are hunted for food throughout Europe, but relatively few for example in most of their range, both by indigenous Greenland and Iceland. A few long term people and sportsmen. Collecting eider studies, especially from Britain, the eggs for food was formerly widely Netherlands, and Fennoscandia form the practised, but is nowadays virtually basis of our understanding of eider confined to the natives in N-America and population biology (e.g., Milne, 1974; Greenland. Collecting down from nests Coulson, 1984; Mendenhall & Milne, was similarly a common practice, but 91

1985; Swennen, 1991; Hario & Selin, been little studied in most populations. 1995). In Britain, on average over 20% of As the eider is a colonial nester and females were non-breeding each year (0- generally tame on the breeding grounds, 60%; Coulson, 1984). many studies have focused on various The eiders' reproductive output is aspects of breeding biology. We have a potentially high, the mean clutch size is rather extensive knowledge of eider 4-5 eggs and on average 2-4 young hatch feeding behaviour and food choice; in each nest (Swennen, 1983; Coulson, nutritional status before and during 1984; Hario & Selin, 1988; Skarphedins­ breeding; clutch size, incubation, hatch­ son, 1993). Duckling survival is usually ing success, and variation in duckling very low, on average, less than 10% of survival. Furthermore, population esti­ ducklings survive through fledging mates are getting better and some popu­ (Milne, 1974; Hario & Selin, 1991; lations are satisfactorily monitored. Swennen, 1991). Most losses are within Among gaps in our knowledge of 7 days of hatching (Swennen, 1989). eiders are the ultimate reasons for long Typical reproductive losses of eiders term population changes in areas where during the breeding season in Iceland are over-harvesting is not a problem, for illustrated in Fig 1. example in the Baltic, Britain, and Eider duckling survival and subsequ­ Iceland. In fact, to date we do not have a ent juvenile survival rates are by far the good model for any eider population. most important regulating factors con­ Furthermore, much remains to be learned trolling eider fecundity and outweigh all about the importance and interaction of other factors operating during the eiders' nutritional status, parasites, diseases, and nest-stage. Gulls appear to prey mostly predators on eider duckling survival. on weaklings, i.e. young that are emaci­ In this paper I will discuss some of ated by diseases, parasites, and hunger. the eider's life history traits and how In addition, gulls do not prey on young they relate to different traditions in that are more than 17 days old utilising this abundant species. A special (Mendenhall & Milne, 1985). Ducklings emphasis will be placed on eider utilisa­ do not appear to survive better in areas tion in Iceland. Comments from J an Ove where there is little or no gull predation Bustnes improved this paper. (Mendenhall & Milne, 1985, Hario & Selin, 1989, 1991; Swennen, 1989, Eider population dynamics 1991). There is a certain discrepancy in the Proximate causes of eider duckling eider's life history; their potentially high deaths are diseases, parasites, and pre­ fecundity is typical of a waterfowl. Adult dation by gulls. In an Icelandic study, eiders, however, have high survival gulls reportedly took more than half of annual rates, typical of a seabird, or 90- the young lost before fledging (J. Gud­ 95% in non-harvested populations mundsson, pers. comm.). Hario & Selin (Baillie & Milne, 1982; Coulson, 1984). ( 1995) recorded extremely low repro­ The ratio of eiders breeding annually ductive output of eiders in the Gulf of is highly variable, most probably influ­ Finland. They identified nutritional and enced by the females nutritional status physiological factors as the most pro­ before the breeding season. Non­ bable causes for the low duckling survi­ breeding of sexually mature eiders has val rate and eliminated the controlling 92

Eggs

Ill Onundarfj6r6ur D Dyrafj6r6ur 4

3

2

0 Max clutch At hatch 25 July Initiation of laying 1 July

Fig. 1. Eider reproductive parameters in two fj ords in NW-Icelandin 1985 (eggs and young per female). From Skarphedinsson (1993). role of gulls and parasites. According to Estimating eider duckling survival Galaktinov (in this issue) the White-Sea and the role of predators, diseases etc. in eider population fluctuates perennially regulating and controlling the reproduc­ due to the effects of helminth infestati­ tive output is complicated (Fig 2.) and ons. If this is true, it would be the sole requires co-operation among scientist, example of parasites regulating an eider crossing both national and disciplinary population. borders.

Food Nutritional availability Parasites status

' Bacteria Yo ung Viruses fledged

ather, We ... Gulls environmental accidents

Fig 2. Factors effecting eider duckling survival. 93

Some problems in t•ider population annual killing of tens of thousands of management. gulls, ravens, mink, and foxes. Most citkr jH >pulat i(lllS are shared by Utilisation of eiders more than one l' tHIIltry. hence eider Eider utilisation can roughly be conservation dt•pcnds (lJl international divided into three categories: (1) Eiders co-operation and :t)',n'clllt'nts. As eiders are hunted for food, both by indigenous occur in laq.•.e ClHH'l'lltralions, they are people and sportsmen. (2) Collecting susceptihlt• to lnass deaths due to oil eider eggs for food was formerly widely spills, poisoning, dist•ast�s. etc. Northern practised, but is nowadays virtually eider populations arc poorly known, for confined to the natives in N-America example in nort lwm ( 'anada and Green­ and Greenland. (3) collecting down from land where ovt· r lwrvc·.still)!, seems to nests was similarly a common practice. constitute a st•riotts prollkm (Krohn et Besides, eiders have aestethic value and al. , 1992; Wohl, JlJ%). are an important topic of research. During till' J

Kilograms 5.000 ,------,,------, 0 Maximum 1:1 To day 4.000 1------.-.------·--··------1 L______J

3.000 f------�-·---1

1.000 1------�--j

O l_L--'-L_l-""""""--'� Canada Iceland Norway Greenland Svalbard Russia

Fig. 3. Eider down harvest during the 19th and 20th centuries. (Various sources; Skarphedins­ son, unpubl. material). contrary to the situation in less populated • Protection of the breeding grounds areas (Reed, 1986). The eider has been from human intrusions. protected and managed in Iceland since • Eiders are attracted/lured to nest in the 1200s, initially for egg collecting, but dense colonies. later for down harvesting. Eider down became an important commercial item in • Reduction of predators in the vicinity the 1600s and 1700s, and ever since, of the colonies - subsidised by the Iceland has been a leading producer municipalities and the government. (Doughty, 1979). Methods of collecting the eider down Eider down is an expensive commo­ are virtually the same as during the 18th dity; the world-market price is about and 19th centuries (Kristjansson, 1986). $750/kg, and relatively little effort and The colonies are carefully searched for cost is involved in harvesting and nests, usually in late May to mid-June. processing the down compared to other The down is taken from each nest, either farming practices. Even in modern times, during late incubation or after hatching. many farmers in Iceland earn the majo­ In the first instance it is usually replaced rity of their income by eider husbandry. with hay or grass. In addition, eider husbandry often keeps The methods in processing the down isolated farmsteads, which are not sui­ have changed somewhat - the main table for modern livestock farming, from change being the introduction of electric being abandoned. The estimated export machines to clean the down. The first value of eider down from Iceland in stage of cleaning is still the same, na­ 1990 was about $2.4 million, but it has mely drying the down outdoors in the since decreased somewhat due to marke­ sun and the gentle breeze of summer. ting problems (Skarphedinsson, 1994). Between 1900 and 1940 the mean Eider husbandry in Iceland basically annual recorded eider down harvest in involves the following practices: Iceland was about 3,600 kg/yr., reaching Collection of eider down. a peak in 1915 (4,300 kg; Fig. 4). From • the 1930s to the early 1960s, the harvest 95

Kg 5.000 ,------, f------1polar ice drift 4.000

3.000 �

2.000

1.000

0 1875 1900 1925 1950 1975 1995

Fig. 4. Eider down harvest in Iceland, 1870-1 995 (5-year running means). Based on Smebjorns­ son (1996) and information supplied by the Statistical Bureau of iceland. gradually decreased to about 1,800 kg/yr. The consensus of many eider farmers (Gudmundsson, 1941; Doughty, 1979; is that increased predation by pests such Smebj i)rnsson, 1996). Since the early as great black-backed gull Larus mari­ 1980s, however, eider down harvest has nus, common raven Corvus corax, and increased considerably. About 3,000 the introduced mink Mustela vison kilograms of eider down are now produ­ caused the decline in eider down harvest ced annually in Iceland and mostly from the 1930s to the 1970s. The lack of exported to Germany and Japan where it labour to harvest the down has also been is used in luxury bedcovers. The down implicated (Doughty, 1979; Gardarsson, harvest seems to have been relatively 1982). Similarly, the recent increase in stable since about 1989 (Skarphedinsson, down yield is attributed by some to 1994). The ultimate reasons for the increased pest control. None of these improved down yield are largely explanations for fluctuations in the down unknown. harvest have been verified with experi­ On average, 60 eider nests yield one ments or field data. kilogram of down (Gudmundsson, 1941). Current eider husbandry practices in Assuming a constant harvest effort, the Iceland appear to be extremely effective harvestable eider population in Iceland in maintaining a high nest success (84% declined from about 260,000 pairs in NW-Iceland in 1985; Skarphedinsson, around 1928 to about 110,000 pairs 1993). Some eider farmers, however, around 1960. The current harvested regard any and all egg predation u­ population has now risen to about nacceptable and their goal is to eliminate 200,000 pairs, but the total Icelandic potential predators rather than to control population is probably around one milli� damage. For managing eider colonies for on birds, including non�breeding adults maximum economic returns it is more and immatures (Skarphedinsson, 1994). important to protect the producing ------··· -·······-· ···

96

females from predators (mainly fox and Gudmundsson F. [Eider husbandry and down mink) and human-induced mortality production in Iceland. Reykjavik: A report to factors (e.g., oil pollution and accidental the Icelandic Parliament, 1941 (in Icelandic) catch in fishing nets) rather than attemp­ Hario M, Selin K. Thirty-year trends in an ting to eliminate all egg predation in the eider population: timing of breeding, clutch colonies. size, and nest preferences. Finn Game Res 1988; 45: 3-10 Conclusion Hario M, Selin K. [Mortality in and the Eider utilisation and management in impact of gull predation on Eider ducklings the future will probably follow the trends in the Gulf of Finland]. Suomen Riista 1989; of the past decades; harvesting eggs and 35: 17-25 (in Finnish) down will become even rarer than today, Hario M, Selin K. [Where have all the Eider but the pressure from hunters to harvest ducklings gone?]. Suomen Riista 1991; 37: eiders as game will undoubtedly increa­ 35-43 (in Finnish) se. Managing eiders for down harvest Hario M, Selin K. Cohort-specific differen­ should focus on improving adult survival ces in reproductive output in a declining rates and nest success. As many hunted Eider population. Danish Rev Game Bioi eider populations are over-harvested, the 1995; 14: 5 emphasis should be given on reducing hunting related mortalities, either by Hario M, Selin K, Soveri T. [Is there a protecting eiders or by strict bag limits. parasite-induced deterioration in eider fecundity?]. Suomen Riista 1992; 38: 23-33 Managing eiders as a game species on a (in Finnish) sustainable bases requires long-term monitoring and hunters should be encou­ Heubeck M. Moult flock surveys indicate a raged to shoot immatures rather than the continued decline in the Shetland Eider adults. population, 1984-92. Scott Birds 1993; 17: 77-84 References Krohn WB, Corr PO, Hutchinson AE. Status Bail lie SR, Milne H. The influence of female of the American Eider with Special Referen­ age on breeding in the Eider Sornateria ce to Northern England. Washington DC: rnollissirna. Bird Study 1982; 29: 55-66 Fish and Wildlife Research, No. 12. U.S. Fish and Wildlife Service, 1992 Coulson JC. The population dynamics of the Eider Duck Sornateria rnollissirna and evi­ Kristjansson L. fslenskir sjavarhcettir. Vol. 5. dence of extensive non-breeding by adult Reykjavik: B6kautgafa Menningarsj6ds, ducks. Ibis 1984; 126: 525-43 1986 (in Icelandic) Doughty RB. Eider husbandry in the North Mendenhall VM, Milne H. Factors affecting Atlantic: trends and prospects. Polar Record duckling survival of Eiders Somateria mollis­ 1979; 19 (122): 447-59 sirna in northeast Scotland. Ibis 1985; 127: Franzmann N-E. Status of the Danish bree­ 148-58 ding population of the Eider Sornateria Milne H. Breeding numbers and reproductive mollissima 1980-83, with notes on general rates of Eiders at the Sands of Forvie Natural population trends in northern Europe. Dansk Reserve, Scotland. Ibis 1974; 116: 135-54 Orn Foren Tidsskr 1989; 83: 62-7 Noer H, Clausager I, Asberg T. The bag of Gardarsson A. [Waterfowl]. In: Gardarsson Eider Somateria mollissima in Denmark A, ed. [Birds]. Reykjavik: Rit Landverndar 1958-1990. Danish Rev Game Bioi 1995; 14 1982; 8: 77-116 (in Icelandic) 97

Reed A, Erskine AJ. Populations of the Common Eider in eastern North America: their sizes and status.In: Reed A, ed. Eider Ducks in Canada. Ottawa: Can Wild! Serv Rep Ser 1986; 47: 156-162 & 172-5 Reed A. Eiderdown harvesting and other uses of Common Eiders in spring and summer. In: Reed A, ed. Eider Ducks in Canada. Ottawa: Can Wild! Serv Rep Ser 1986; 47: 138-46 Skarphedinsson KH. Ravens in Iceland: population ecology, egg predation in eider colonies, and experiments with conditioned taste aversion. MSc.-thesis, University of Wisconsin - Madison, 1993 Skarphedinsson KH. [Sea Eagle Depredation in Eider colonies]. Reykjavik: Ministry of the Environment, 1994 (in Icelandic) Sncebji:irnsson A. [Utilisation of Eiders in Iceland]. B liki 1996; 17 (in Icelandic, in print) Swennen C. Reproductive output of Eiders Somateria m. mollissima on the southern border of its breeding range. Ardea 1983; 71: 245-54 Swennen C. Gull predation upon Eider ducklings; destruction or elimination of the unfit? Ardea 1989; 77: 21-45 Swennen C. Fledgling production of Eiders Somateria mollissima in the Netherlands. J Orn 1991; 132: 427-37 Wohl K. (compiler). International eider conservation strategy and action plan. Report by the Circumpolar Seabird Working Group (draft). Conservation of Arctic Fauna and Flora (CAFF), 1996 Bull Scand Soc Parasitol 1996; 6 (2): 98-102

WHY SHOULD MARINE AND COASTAL BIRD ECOLOGISTS BOTHER ABOUT PARASITES?

Arne Skorping Department of Ecology/Zoology, IBG, University of Tromso, N-9037 Troms0, Norway.

Ecologists studying marine and Here I will focus on two important coastal birds have tended to ignore the areas of seabird research where parasi­ importance of parasites, both at an tism is highly relevant: Studies of life individual and at the population level. histories, and conservation biology. This is certainly not because parasites Parasites and host life histories are rare or absent from this group of hosts, on the contrary, many seabirds The aim of life history studies is to tend to acquire a large number of para­ understand what ecological factors sites due to their broad diet and large determine individual investment in geographic range. To take but one ex­ growth, reproduction and future survival. ample, in the common gull, Larus canus, Many seabird species have a long repro­ a total number of 69 species of digene­ ductive life span, and decisions on how ans, 32 cestode species and 26 nematode much resources should be spent on each species have been recorded (Bakke, reproduction will have a significant 1972). Some of these species are not affect on the lifetime reproductive restricted to the common gull but may success. Intuitively one would expect infect many different host species. that being infected with a parasite would Marine bird parasites may have an affect a bird's decision on when to re­ exceptional wide host range, where the produce and how much resources should digenean Cryptocotyle lingua being able be spent. Yet, parasitism is rarely inclu­ to infect both birds and mammals is one ded as a factor in life history studies. extreme example. Some of the parasites As pointed out by Forbes (1993) recorded from marine and shorebirds are general life history theory predicts that known to be able to produce severe hosts should minimize the impact of disease and increase the mortality rate of parasites by changing their investment in their hosts, but in addition to their pat­ reproduction. Exactly how a host's hological effects, parasites may affect reproductive investment will change many other aspects of the host ecology, depends on the relative impact of the including migratory behaviour (McNeil, parasite on current versus future repro­ 1996), timing of moulting (Langston & duction. A short-lived parasite will Hillgarth, 1995), and nesting behaviour primarily have an effect on the host's (Duffy, 1991). current reproduction, and hosts should  �------�--��------

99

adapt to such parasites by reducing their consequence it will be exposed to a large reproductive investment. On the other number of food-transmitted parasites. To hand, if the host is infected with a long­ examine whether parasitism affected the lived parasite which initially has no or a eiders reproductive success, we shot 34 negligible reproduction, but may have a females shortly before the start of incu­ rapid growth and reproduction at some bation, and measured fat content and later stage, the host should respond by parasite intensities (Skorping & Wareli­ increasing its reproductive investment us, unpublished). We also measured the (Forbes, 1993). Here I will present the diameter of the largest ovarian follicle in results of a study which suggests that the order to assess how close each bird was reproductive response also depends on to laying. The dominant parasites were the ability of the host to tolerate parasi­ digeneans, the acanthocephalan Profilli­ tism. collis botulus and the nematode Amido­ The common cider (Somateria mol­ stomum anseris. Within the whole lissima) does not cat at all during incu­ sample there was a significant negative bation and is therefore totally dependent correlation between body lipid of the on stored nutrient reserves. To build up eiders and the abundance of both dige­ the necessary reserves it has a high neans and nematodes (Table 1). Howe­ feeding rate before incubation, and as a ver, when the sample was split into two

Table I. The correlation between percentage body fat and the number of parasites of three different groups of intestinal helminths in adult female eiders

Abundance Correlation with body lipid r p

Pr()/illicollis ho/1/lus 38.9 -0. 16 0.92 Amidostomum anseris 24.3 -0.37 0.03 Digenea 7381 -0.45 0.01

groups based on the median of the frequ­ small follicles (late layers, Table 2). ency distribution of the egg follicles, we Apparently, there is a relationship found no relationship between body lipid between the timing of breeding in this and parasite intensities in eiders with bird species, and the extent to which it is large fo llicles (early layers) but still a able to build up the necessary lipid significant association among eiders with stores in the presence of parasites. It is Table 2. Correlation between percentage body fat and the number of Amidostomum anse­ ris and digeneans in early- and late-breeding eiders.

Parasite group Abundance Correlation with bod� liJ2id r Early breeders Amidostomum anseris 23.7 0.03 0.91 Digenea 10454 -0.2 0.47 Late breeders Amidostomum anseris 28.8 -0.64 0.01 Digenea 6181 -0.64 0.01 100

also generally assumed that in most bird to 1990. However, there is no consistent species there is a close association trend in the total number of tern nests in between the timing of egg-laying and the same period. This is because the reproductive success (Perrins, I 970). number of nests per colony has increased The ability to tolerate parasites may in the remaining colonies (Fig. I). therefore be a major factor determining reproductive success. Parasites and conservation of marine m 30 and shorebirds Q) • '2 • 0 25 • Many coastal and marine bird species 0 • 0 - • • have shown large variations in breeding • 0 20 • • • densities during the last decades ( ci • • • • • c: et al, I 981 ). Environmental disturbance 15 � and loss of suitable habitats have had a 0 1- negative effect, but increased protection 10 1975 1980 1985 1990 of breeding grounds and feeding habi­ tats, and reduced hunting have been favourable to many species. Usually the optimal habitats are protected, while more marginal ones tend to be used for 200 > • • • • recreation, industry or other human c: 160 • 0 activities. The total number of suitable 0 • 0 120 .... • habitats has therefore shown a steady Q) • • Q. • • 80 • • • decrease during this century. In the $ • m United States it has been estimated that Q) 40 more than 40% of the wetland areas have z 0 disappeared (Sanderson, 1978). How has 1975 1980 1985 1990 this fragmentation of habitats affected bird populations on the remaining areas? If population size is not regulated by Fig. 1. The change in the total number of space as such, but by other factors such colonies and in the number of nests per as food, one would expect the populati­ colony in New Jersey (redrawn from Burger ons of many bird species to increase, and Gochfeld, 1991). both in wintering habitats, in areas used For species like gannets, puffins, during migration, and in breeding habi­ shags and kittiwakes, Furness and tats. Although several studies indicate Birkhead (1984) showed that breeding that many shorebirds have increased densities at a particular colony tended to during the last century (i.e. Evans et al., decrease with increasing densities of 1984), there are very few which also other colonies within range. The reason have tried to estimate the change in for this is probably more competition for available habitats. One of the best studi­ a common food resource, but the effect es in this respect is by Burger & Goch­ is that higher local population densities feld (1991). The number of colonies increase when suitable colonies becomes occupied by the common tern (Sterna scarcer. For some marine and coastal hirundo) in Barnegat Bay, New Jersey bird species there is therefore empirical has shown a steady decrease from 1974 data that confirm our expectation that 101 local density should increase with a When areas used during over­ decline in the number of habitats. wintering and migration become scarcer Parasites are relevant to this situation we would also expect higher bird diver­ because their transmission depends on sity on the remaining ones. Since many host density. For a parasite to be able to marine parasites have a low host specifi­ exist within a host population it requires city this could facilitate the transmission a certain minimum host density, often of parasites between different hosts. called the threshold density. This thres­ Together with more environmental stress hold depends on a number of host- and which may affect host resistance, these parasite-related factors, including para­ ecological changes may increase the site virulence and transmission. For a possibility of epidemic outbreaks of directly transmitted microparasite, such pathogenic parasites. Both behavioural, as a virus, a bacterium and many pro­ population and conservation biologists tozoans, the relationship between the should therefore care about parasites m host threshold density (N1) and some of marine and coastal birds. these factors, can be described as: References N t = (a + b + v) /b Bakke TA. Check list of helminth parasites where: a = parasite virulence, b = natural of the common gull (Larus canus L.). Rhi­ host death rate, v = recovery rate and b = zocrinus 1972; 8: 1-20 parasite transmission rate (May, 1983). Burger J, Gochfe1d M. The common tern: its Note that both more virulent parasites breeding biology and social behaviour. and parasites with lower transmission Columbia University Press, 1991. rates will require a higher host density to Evans PR, Goss-Custard JD, Hale WG. be able to establish in the host populati­ Coastal waders and wildfowl in winter. on. In bird populations where local Cambridge University Press, 1984 density increases we would therefore expect that more parasite species will be Duffy DC. Ants, ticks and nesting seabirds: able to establish, and also that some of dynamic interactions? In: Loye JE, Zuk M, these will tend to be more virulent. This eds. Bird-parasite interactions: ecology, situation is illustrated in Fig. 2. evolution and behaviour. Oxford University Press, 1991: 242-57 Forbes MRL. Parasitism and reproductive effort. Oikos 1993; 67: 444-50

- High virulence Furness RW, Birkhead TR. Seabird colony No. of distributions suggest competition for fo od parasite species supplies during the breeding season. Nature 1984; 311: 655-6 'If-- Lowvirule nce Gray CA, Gray PN, Pence DP. Influence of social status on the helminth community of late-winter mallards. Can J Zoo! 1989; 67: Host density 1937-44 Fig. 2. The relationship between host density Langston N, Hillgarth N. Moult varies with and the number of parasite species that will parasites in Laysan Albatrosses. Proceedings be able to establish in the host population. At of the Royal Society of London Series B higher host density we will also expect more 1995; 261: 239-43 virulent parasites. 102

May RM. Parasite infections as regulators of animal populations. American Scientist 1983; 71: 36-45 McNeill R, Diaz MT, Casanova B, Villeneu­ ve A, Thibault M. Trematode infestation as a factor in shorebird oversummering: A case study of the greater yellow1egs (Tringa melanoleuca). Bull Scand Soc Parasitol 1996; 6: 114-7 Perrins CM. The timing of birds breeding seasons. Ibis 1970; 112: 242 - 55 Sanderson GC. Conservation of waterfowl. In: Bellrose FC, ed. Ducks, geese and swans of North America. Harrisburgh: Stackpole Books, 1978: 43-58 Bull Scand Soc Parasitol 1996; 6 (2): 103-113

ECOLOGICAL IMPLICATIONS OF HEMATOZOA IN BIRDS

G. Valkiunas Institute of Ecology, Lithuanian Academy of Sciences, Akademijos 2, Vilnius 2600, Lithuania

Hematozoa of birds have been objects Kingdom Protista (Haeckel, 1866) of intensive scientific research over a Phylum Sporozoa (Leuckart, 1879) 100 year-period and about 45 per cent of ( =Apicomplexa Levi ne, 1970) the bird species (>21 0 000 specimens) Class Coccidea (Doflein, 1901) have been investigated for blood parasi­ Subclass Coccidia (Doflein, 1901) tes. Data on blood parasites are available Order Haemosporida (Danilewsky, for most of the ecological bird groups 1885) (Herman et al, 1976; Bennett et al, 1981; Bishop & Bcnnett, 1992). From an Family Haemoproteidae Doflein, ecological point of view, one results of 1916 significance is the description of the Genus Haemoproteus Kruse, 1890 general pattern of distribution of hema­ Family Plasmodiidae Mesnil, 1903 tozoa in nature. The aim of this paper is Genus Plasmodium Marchiafava et to highlight the ecology of haemospori­ Celli, 1885 dian parasites (Sporozoa: Haemosporida) Family Garniidae Lainson, Landau et of wild birds. This group of bird hema­ Shaw, 1971 tozoa has especially wide distribution Genus Fa llisia Lainson, Landau et and has been investigated particularly Shaw, 1971 well. Family Leucocytozoidae Fallis et Haemosporida of birds are obligate­ Bennett, 1961 heteroxenous parasites which use blood­ Genus Leucocytozoon Berestneff, sucking Diptera (Culicidae, Cerato­ 1904 pogonidae, Simuliidae, Hippoboscidae) as final hosts and vectors. The life cycles Diagnostics of Haemosporida by blood of the parasites have been reviewed film survey (except Garniidae; see Seed & Manwell, The vast majority of ecological 1977; Gabaldon et a!, 1985; Atkinson & investigations of haemosporidian of van Riper, 1991; Desser & Bennett, birds are based on microscopy of blood 1993). smears. In temperate regions, this met­ The accepted systematic position and hod provides good results only during classification of the bird Haemosporida warm period of a year when the parasites are: are available in blood. A relapse occurs 104 approximately at the beginning of the autumn. The period of chronic parasite­ breeding period, and the parasitemia, as mia of Haemoproteus is longer than a rule, lasts during the period when the Plasmodium, however, gametocytes of newly hatched young generation can be most species of Haemoproteus disappear infected. The best period for blood from the blood at autumnal migration. investigation is accordingly May-July in Extensive search of blood smears may the Northern part of Holarctic. During only reveal a few gametocytes of Leuco­ this period, the blood smears give good cytozoon throughout late autumnal results for diagnostication of Haemo­ migration and in winter. Birds, infected proteus and Leucocytozoon. For Plas­ with Plasmodium and Haemoproteus modium is the period of acute infection usually cannot be recorded during late very short with only a few parasites are autumnal or early spring migration by present in the blood during a chronic blood film surveys, but Leucocytozoon is parasitemia. An extensive search of often registered. That is why the data on blood films is necessary, however, not prevalence of infection, which are based always enough to detect a present Plas­ on the method of blood film microscopy, modium infection. Inoculation of blood should be used critically in ecological from wild birds into susceptible captive investigations of Haemosporida. Immu­ hosts, gives better results but is expensi­ nological methods are applied for esti­ ve. As a rule, the search of blood films mation of the prevalence of infection reveals only a relative picture of distri­ (Graczyk et al, 1994) and promising on bution of malaria. However, for some the level of genus but still inaccurate for purposes, the method is helpful and can parasite species determination. give valuable information on the general Origin of bird Haemosporida and situation in a specific area. distribution by hosts It is important to note that once All families of bird Haemosporida infected, the bird remains infected for occur in reptiles (Table 1). Most likely, life or many years. However, the period haemosporidians of birds are directly of patent infection is seasonally restric­ phylogenetically connected to the repti­ ted and different between species of lian parasites. Of importance for explai­ Plasmodium, Haemoproteus and Leuco­ ning the colonization of birds is firstly cytozoon. In the Northern part of Palae­ the phenomenon that phylogenetically arctic, most species of malarian parasites primitive orders of birds have no hae­ cannot be registered in the blood in mosporidian parasites, or their fauna is

Table 1. Fauna of Haemosporida in vetiebrate hosts.

Class Number of species Haemopro- Plasmodiidae Garniidae Leucocyto- Total teidae zoidea Teleostomi 1 (?) 1(?) 0 0 2(?) Amphibia 3 2 0 0 5 Reptilia 25 69 5 2 Ill Aves 132 38 1 35 206 Mammalia 36 56 0 0 92 Total 197 166 16 37 416 �-� �-����---·�------

105 extremely poor. For example, 4 per cent of bird haemosporidians. Therefore, it of the species of the world fauna of bird seems that the reptilian parasites incor­ Haemosporida have been registered in porated the birds at a relatively late the orders Sphenisciformes, Sthruthioni­ period of evolution of A ves when the formes, Rheiformes, Casuariiformes, Ap­ principle orders of contemporary birds terygiformes, Tinamiformes, Gaviifor­ already have appeared and diversified. mes, Podicipediformes, Procellariifor­ Probably, this process took place ap­ mes, Pelecaniformes. It is likely, that the proximately at Eocene-Oligocene, or initial evolution of bird Haemosporida is even later (Darlington, 1957). It is im­ not connected with the above-mentioned portant to note that all groups of vectors groups of Aves. Secondly, especially of bird Haemosporida existed at that rich fauna of Haemosporida is a dis­ time. The process could take place at the tinctive feature of the phylogenetically warm intracontinental regions where the relatively young orders of the birds, that reptilian haemosporidians are widely is Passeriformes, Galliformes, Columbi­ distributed. It is very likely that blood­ formes, Coraciiformes and Piciformes sucking dipteran vectors transmitted (Table 2) with 84 per cent of the species Haemosporida from reptiles to birds, as

Table 2. Fauna of Haemosporida of birds of different orders.

Order Number of species Haemo- Plasmodium Fallisia Leucocyto- Total rote us zoon 1. Sphenisciformcs 0 2 0 3 2. Struthioniformcs 0 0 0 1 1 3. Tinamiformcs 0 3 0 0 3 4. Pelccaniformcs 0 1 0 I 2 5. Ciconiifonncs 4 4 I 2 11 6. Anseriformcs 2 9 0 12 7. Falconiformcs 6 5 0 12 8. Gallifonncs 9 17 0 7 33 9. Turniciformes 0 1 0 0 10. Gruiformcs 5 8 0 1 14 11. Charadri i formes 5 2 0 2 9 12. Columbiformcs 6 11 1 1 19 13. Psittaciformes 2 5 0 0 7 14. Cuculifonncs 2 0 4 15. Musophagiformes 0 3 16. Strigiformcs 2 5 0 8 17. Caprimulgiformes 1 3 0 1 5 18. Apodiformes 4 3 0 0 7 19. Coliiformes 0 0 1 2 20. Trogoniformes 0 0 0 21. Coraciiformes 10 4 0 4 18 22. Piciformes 9 8 0 1 8 23. Passeriformcs 63 16 0 7 86 106 well as distributed the parasites among riidae, Hydrobatidae, Pelecanoididae, different orders of A ves. It is interesting Phaethontidae, Sulidae, Phalacrocoraci­ that 42 per cent of the species of the bird dae, Anhingidae, Fregatidae, Stercorarii­ Haemosporida occur in Passeriformes. dae, most of Laridae, Rynchopidae, This indicate a rapid diversity of Hae­ Alcidae). It is important to note that mosporida in phylogenetically young seabirds are susceptible to haemospori­ groups of birds. dosis and suffer from the diseases. Acute and often fatal epizootics of avian mala­ Marine and coastal birds have evol­ ria (Plasmodium relictum and P. elon­ ved and live in areas where reptilian gatum) among penguins in zoos is an haemosporidian parasites are absent. example (Cranfield et al, I 990). This And they are also ecologically isolated fact indicates that haemosporidosis from the haemosporidians, because the restrict the penetration of hydrophilous birds inhabit territories with relatively birds into intracontinental territories. cold or windy climatic conditions where dipteran vectors are absent, inactive or Distribution of species of Haemospo­ appeared historically late. This explain rida in birds of different orders is shown the exceptionally poor fauna and low in Table 2. Passeriformes (86 species), prevalence of Haemosporida in all Galliformes (33), Columbiformes (19), groups of marine and coastal birds, or Coraciiformes and Piciformes (I8) have other hydrophilous birds (e. g., Gaviidae, an especially diversed fauna of Hae­ Podicipedidae, Diomedeidae, Procella- mosporida. An especially rich fauna of Table 3. Fauna of Haemosporida of birds in order Diptera.

Family and genus Number of described species Haemopro- Plasmodium Leucocy­ Total teus tozoon Simuliidae Austrosimulium 0 0 Cnephia 0 0 4 4 Prosimulium 0 0 7 7 Simulium 0 0 12 12 Ceratopogonidae Culicoides 7 0 8 Culicidae Aedes 0 5 0 5 Anopheles 0 5 0 5 Armigeres 0 1 0 Culex 0 15 0 15 Culiseta 0 6 0 6 Mansonia 0 3 0 3 Psorophora 0 0 Wy eomyia 0 0 Hippoboscidae Microlynchia 0 0 Ornithomyia I 0 0 1 Pseudolynchia 3 0 0 3 ------�--

107

Haemoproteus has been registered in nia of Plasmodium and Simulium, Pro­ Passeriformes (63 species), Plasmodium simulium and Cnephia of Leucocy­ in Galliformes ( 17) and Passeriformes tozoon. Vectors of bird Fa llisia (family (16) and Leucocytozoon in Passeriformes Garniidae) are still unknown. (7). Haemosporida have so far not been . Geographical distribution registered in Casuariiformcs, Apteryg ­ � Haemosporidian parasites of birds are formes, Phoenicoptcri formes, Eurypygi­ distributed all over the world, except the formes and these parasites are uncom­ Antarctic (Tables 4, 5). Haemoproteidae, mon and undetermined to the species Plasmodiidae and Leucocytozoidae have level in the Rhciformcs, Gaviiformes, a world-wide distribution, Garniidae Podicipediformcs, Proccllariiformes and have been found only in the Neotropics. Cariamiformes. Rich fauna of the hae­ The faunae of the Holarctic (123 speci­ mosporidians in the phylogenetically es), Ethiopian ( 108) and Oriental ( � 06) young orders of birds and poor fauna of . zoogeographical regions, are esp c1ally the parasites in the phylogenc�Ically Id � . ? rich. A total number of the species of orders arc main features ol. d1stnbutwn Haemoproteidae, Plasmodiidae and of Haemosporida in vertebrate hosts. Leucocytozoidae, which have be n This can be explained by: (i) relatively � found in a vast territory of the Holarct1c, recent penetration of the parasites into Ethiopian and Oriental regions, makes birds, (ii) ecological isolation from up 92, 79, and 100 per cent, respectively, vectors of some phylogenetically old of the world fauna of the above­ orders of A ves, and (iii) richness of most mentioned families. The faunae of the of the evolutionary young orders of birds Australian (22 species) and Neotropical from the point of view of quantity and (52) zoogeographical regions, are much diversity. poorer. The data on vectors of bird Hae­ The fauna of the Australian region is mosporida arc summarized in Table 3. especially scanty. Proba�ly, the h e­ According to the current knowledge, � mosporidians penetrated m t�e regiOn dipterans of genus Culicoides are vectors relatively not long ago. In spite f t�e of most species of J-laenwproteus; Culex, � poverty, the fauna of the Neotrop1cs Is Culiseta, Aedes, Anopheles and Manso-

Table 4. Fauna of Hacmosporida of birds in different zoogeographical regions.

Zoogeographical region ------����xNumber of spec::::.::::::::.._ies _____ -:=----:-- Haemopro- Plasma- Fallisia Leucocyto- Total teus diu m zoon - Holarctic 78/24 19/6 0 26/9 123/39 Ethiopian 70/17 13/2 0 25/6 108/25 Oriental 70/11 20/8 0 1611 106/20 Australian 1111 3/0 0 8/0 2211 Neotropical 28/9 18/8 1/1 5/0 52118 Antarctic 0 0 0 0 0

Note. A total number of species is given in numerator, and t�e nu ber of species, whic� have � . . been registered only in a certain zoogeographical regiOn, IS given Ill denommator. 108

Table �· Prevale�ce of Haemosporida in birds of diffe rent zoogeographical regions (accordmg to Gremer et a!, 1975; McCiure et a!, 1978; White et a!, 1979; Peirce, 1981, and new data).

Zoo geographical Examined Infected region Haemop_roteus Plasmodium Leucocytozoon n % n % n % Holarctic 102590 18363 17.9 298 1 2.9 16619 16.2 Ethiopian 11507 1887 16.4 368 3.2 526 4.6 Oriental 45091 5926 13.1 348 0.8 1327 2.9 Neotro2ical 54101 3841 7.1 865 1.6 66 0.1 Note. Data on microscopy of blood smears are included only. Precise data on Australian region are not available. clearly different from the Australian one: grations of birds to the southern latitu­ firstly, the number of the species of des, characterize the Holarctic zoogeo­ Plasmodium is 6 times larger in the graphical region as a contemporary Neotropical region which is very close to centre of spread of Leucocytozoidae. On the Holarctic, Ethiopian and Oriental the contrary, the vast territory of the situation. Secondly, the impoverishment Ethiopian, Oriental and Neotropical of the Neotropical fauna of Haemospori­ zoogeographical regions is distinguished da, which is largely a result of decrease by: (i) rich fauna of Plasmodium, (ii) of the fauna of Leucocytozoon. Only high prevalence of infection of birds cosmopolitian species of the parasites with the parasites, and (iii) regular visits have been discovered in the Neotropics ( of a lot of holarctic birds. This territory e. g. Leucocytozoon danilewskyi, L. dub­ can be regarded as a centre for distribu­ reuili, L. fringillinarum, L. marchouxi). tion of malaria parasites of birds. The In addition, the prevalence of infection relatively high prevalence of Plasmodi­ of birds with Leucocytozoon is extremely um in the Holarctic, in part, can be low in the Neotropical region (Table 5). explained by infection of birds at winte­ The facts testify to the second-nature ring places (Valkiunas, 1993b) Garnii­ origin of the Leucocytozoon fauna in the dae have been found in birds only in the Neotropical region. The extremely poor Neotropical region, which is a centre of fauna of Leucocytozoon and presence of distribution of the parasites. Fallisia, are main features of the fauna Most species of bird Haemosporida of bird Haemosporida in the Neotropics. have areas covering several zoogeograp­ Fallisia neotropicalis is the sole species hical regions. For example, 54 per cent of Garniidae which have been registered of species of Haemoproteus have been in birds (Gabaldon et a!, 1985), and found in more than one zoogeographical endemic to the Neotropical region. region, 59 per cent of Leucocvtozoon The Holarctic is distinguished by and 37 per cent of Plasmodium . . · A total especially high prevalence of infection number of species which areas cover of birds with Leucocytozoon (Table 5). A approximately 3-4 zoogeographical combination of such factors as: (i) rich regions, makes up 25 per cent of the fauna of Leucocytozoon, (ii) high preva­ world fauna of bird Haemosporida. lence of infection of birds with the Haemoproteus nettionis, H. noctuae, H. parasites and (iii) regular seasonal mi- passeris, H. plataleae, Leucocytozoon �'���. �------

109 danilewskyi, L dllln l'il/ 11, L Jiingilli­ of Palaearctic-Ethiopian migrants, can be narum, Plasnwdiwn lilt lllil/ln tl/11, P. pointed out (V alkiunas, 1993 b). Seaso­ relictum and P. \'UII,1.;hmn :ur cosmopo­ nal migrations of trans-Saharan migrants litan parasites. 1\ ll'll!lctH y for cosmopo­ do not or only insignificantly increase, litan distribution is the nwin feature of the Palaearctic birds infection with geographical distrilmlton ol bird liae­ Leucocytozoon. As a rule, the infection mosporida. 1\ sunT�;·JHI 1 tllonization of of Palaearctic birds with leucocytozoids the Northem JJqJ;utltt' It'llitor ies is the takes place in nesting areas only. On the second important lcattlll' of dist ribution contrary, the protracted stay of distant of the parasites. l'w •·x;Hnplc, in the migrants in the Ethiopian region contri­ ;·onn si Palaearc I ic, 1 J' tl(< /(' 1'1n mondi butes to the infection of birds with penetrated far llcyund tht· North polar­ Haemoproteus and Plasmodium. The circle and adaptnl Ill tlw circulation distant migrants bring two groups of the under sewn· tlltHlla conditions, thus haemosporidian parasites from wintering providing t·xtn·nwly hi1•.h pwva lence of grounds to the nesting areas. The first infection of birds t Yalkiunas et al, group consists of species which do not 1990). This is a wuqtH' situation for circulate in the north and, as a rule, do Haemospmida. In /',t'IH't:tl, thL: prevalen­ not infect the immature birds, as: Ha­ ce of infectitm ol birds with /,eucocy­ emoproteus hirundinis, Plasmodium tozoon significantly innl'ases in the rouxi, P. fa llax, and others. The second Northern llolarl'lit· in co!llparison to group consists of the species, which tropical n.·ginns. lt can he explained by circulate in the wintering grounds as the high dcnsitie�·; of both hint and vector well as in nesting areas, as: Plasmodium populations and :Hlaptation of the para­ relictum, Haemoproteus belopolskyi, H. sites for tlw dt·vv l'lJJilwnt in vector at balmorali, H. pallidus, which the species low telllpcralllt<'s. Species of Ha­ known. !'lusntoditml emoproft'l/.1' and require The fauna of haemosporidian parasi­ higher tetntll'rattllcs for development tes of the distant Palaearctic-Ethiopian than in zones ol tllndra and forest-tundra. migrants is regularly enriched after birds The role of Sl'asonal migrations in the arrival from wintering grounds, mainly distribution of llat�mosporida of birds at the expense of species of Haemopro­ teus and Plasmodium. However, this The results of long tenn populational process does not change the epizootolo­ studies on the basis of ringed birds gy in the breeding areas as shown by the provide evidence that all genera of relatively stable fauna of haemosporidi­ Haemosporida, except Fal/isia, circulate ans in immature birds uninfected with in the I lolarctic (set� lknnell et al, 1976; parasites of southern origin. The barriers Valkiunas, I

migratory birds, can be estimated as a of chaffinches makes the birds more "preserved" genetic heritage, which is vulnerable to preys and unfavourable being realized very slowly. climatic and feeding factors as well. It implies a reduction in the ability of Peculiarities of influence on wild birds competition and increase probability of Without question, the haemosporidi­ elimination of infected specimens under an parasites are important agents of field conditions. If birds survive the diseases of domestic and some wild bird acute parasitemia, then they may be species in zoological gardens and aviari­ caught in mist nets; (ii) Heavy Ha­ es (Bennett et al, 1993). Also, Ha­ emoproteus sp. infection (> 20 gameto­ emoproteus infection is known to cause a cytes per 1000 erythrocytes) is associa­ gross pathology (Atkinson et al, 1988; ted with reduced accumulation of mi­ Hartley, 1992; Earle et al, 1993). Howe­ gratory fat in passerines during spring ver, the believe of harmlessness of migration. The migratory fat is a main Haemosporida to free-living birds domi­ energetic material for migratory flight. nates in the literature nowadays (Bennett So, a heavy parasitemia due to ha­ et al, 1993). This is predicated upon a emoproteids, cannot be neutral for postulate that the data on serious patho­ migrants; (iii) The prevalence of Leuco­ logy of Plasmodium, Haemoproteus and cytozoon increases in late stages of the Leucocytozoon in wild birds (see, for autumnal migration of chaffinches, example, Karstad, 1965; Stone et al, which may imply that heavily infected 1971; M arcus & Oosthuizen, 1972; birds are delayed in their migration. Herman et al, 1975; Gabaldon & Ulloa, Possibly, this is one of the regulatory 1980; Atkinson & Forrester, 1987; van parasitic mechanisms which is realized Riper III, 1991; Hartley, 1992) are not during the seasonal migrations. It is enough to prove the existence of a direct interesting to note that irruptions of birds pathogenic influence of the parasites on are accompanied by sharp change of free-living populations. parasitocenosis of Haemoproteus, Only negative influence of hae­ Leucocytozoon and Trypanosoma, which mosporidians on wild free-living birds indicate causal relationship between are difficult to obtain due to need for the these phenomena (Valkiunas, 1993a). constant monitoring of infections under The pathogenicity of haemosporidian field conditions. And any lowering of parasites of wild birds is insufficiently competitiveness at the heavy phase of known. To solve the problem, sophisti­ infection under experimental conditions cated methods of population biology is simply not easy to estimate. However, should be elaborated in collaboration the long-term populational investigation between both parasitologists and ornit­ on the Curonian Spit in the Baltic Sea hologists. provides evidence that the hematozoa harm their free-living avian hosts Haemosporidians as biological tags in (Valkiunas, 1993a): (i) During the 3 day bird population studies peak parasitemia of Haemoproteus As a result of the long period of fr ingillae, young chaffinches Fringilla intensive investigations, original data coelebs become less mobile and secreti­ have been accumulated in the ecological ve and are usually absent from mist net parasitology which can be used in adja­ catches (but may be shot). Reduced cent fields of biology. One example is mobility during the peak of parasitemia analysed here. 111

A new method have been suggested groups of birds gives a possibility to for determination of number of inter­ estimate the relative number of inter­ populational dispersals in some popula­ populational dispersals. The conducted tions of birds by using Leucocytozoon as parasitological investigations (Valki­ biological tags. The method can be used unas, 1988; Vysotsky & Valkiunas, in ornithological studies of bird dispersal 1992) have shown that, when migrating in regions isolated by ecological barriers over the Curonian Spit, birds of more where the circulation of Leucocytozoon northern populations, extensively infec­ do not take place (V alkiunas, 1988). For ted with Leucocytozoon, either do not example, on the Curonian Spit and merge with local populations of Fice­ Gothland Island in the Baltic Sea, and dula hypoleuca, Fringilla coelebs, Barsa-Kelmes Island in the Sea of Azov. Hippolais icterina and Phylloscopus A possibility to use the method is stipu­ trochilus or their portion is quite negli­ lated by the following facts. Leucocy­ gible. This phenomenon is indicative of tozoon is a specific bird parasite widely relative stability of the above-mentioned distributed in the Holarctic. Blood­ Curonian populations of birds. On the sucking flies (Simuliidae) are vectors of contrary, the active interchange has been Leucocytozoon. Transmission of the registered between far-distance popula­ parasites is prevented in regions isolated tions of Parus major and Phylloscopus by ecological barriers where breeding sibilatrix. places of simuliids are absent. At such Most likely, other genera of Hae­ places, the fauna of Leucocytozoon mosporida cannot be used in bird popu­ develops by the fo llowing two ways: lation studies as biological tags because firstly, birds of the local origin can bring their vectors (Culicidae, Ceratopogoni­ the parasites from the wintering places, dae) are distributed almost everywhere. secondly, the inhabiting of infected However, the example discussed show birds, migrating over the territory, is fruitful possibilities for collaboration possible. Evaluation on the contribution between parasitologists and adjacent of these two factors in the infection of fields of zoology. birds with Leucocytozoon gives a possi­ bility to use the parasites as biological References tags. For this purpose, at least two bree­ Atkinson CT, Forrester DJ. Myopathy ding groups of birds should be investi­ associated with megaloschizonts of Haemo­ gated at the territory. The first group proteus meleagridis in a wild turkey from consists of ringed birds of known (local) Florida. J Wild1 Dis 1987; 23:495-8 origin, and the second - unknown origin. Atkinson CT, Forrester DJ, Greiner EC. The birds of the local origin can be Pathogenicity of Haemoproteus meleagridis infected with Leucocytozoon only at the (Haemosporina: Haemoproteidae) in experi­ wintering places and migratory route. mentally infected domestic turkeys. J Para­ The birds of unknown origin can be sitol 1988; 74: 228-39 infected at place of birth as well as Atkinson CT, van Riper Ill C. Pathogenicity wintering territories and migratory ways. and epizootiology of avian haematozoa: Prevalence of infection of birds with Plasmodium, Leucocytozoon, and Haemo­ Leucocytozoon increases when birds of proteus. In: Loye JE, Zuk M, eds. Bird­ the second group move into the region. parasite interactions: Ecology, evolution, and Determination of the prevalence of behaviour. Oxford University Press, 1991: infection of Leucocytozoon in these two 19-48 112

Bennett GF, Greiner EC, MF, footed penguins (Spheniscus demersus). J Herman CM. Hematozoos de aves paserifor­ Parasitol 1994; 80: 60-6 mes silvestres muestreadas en anos suce­ Greiner EC, Bennett GF, White EM, Coombs sivos. Bol Dir Malarial San Amb 1976; 16: RF. Distribution of the avian hematozoa of 313-9 North America. Can J Zoo! 1975; 53: 1762- Bennett GF, Kufera J, Woodworth-Lynas C, 87 Whiteway M. Bibliography of the avian Hartley WJ. Some lethal avian protozoan blood-inhabiting Protozoa: Supplement 1. St. diseases of native birds in eastern Australia. John's: Memorial University of Newfound­ Tydskr S Afr vet Ver 1992; 63: 90 land, 1981 Herman CM, Barrow JH, Tarshis IB. Leuco­ Bennett GF, Peirce MA, Ashford RW. Avian cytozoonosis in Canada geese at the Seney Haematozoa: mortality and pathogenicity. J National Wildlife Refuge. J Wild! Dis 1975; Nat Hist 1993; 27: 993-1001 11: 404- 11 Bishop MA, Bennett GF. Host-parasite Herman CM, Greiner EC, Bennett GF, Laird catalogue of the avian haematozoa: Supple­ M. Bibliography of the avian blood­ ment 1 and Bibliography of the avian blood­ inhabiting Protozoa. St. John's: Memorial inhabiting haematozoa: Supplement 2. St. University of Newfoundland, 1976 John's: Memorial University of Newfound­ land, 1992 Karstad L. A case of leucocytozoonosis in a wild mallard. Bull Wild! Dis Assoc 1965; I: Cranfield MR, Shaw M, Beall F, Skjoldager 33-4 M, Ialeggio D. A review and update of avian malaria in the African penguin (Spheniscus Markus MB, Oosthuizen JH. Pathogenicity demersus). Proc Am Assoc Zoo Vet 1990: of Haemoproteus columbae. Trans R Soc 243-8 Trop Med Hyg 1972; 66: 186-7 Darlington PJ. Zoogeography: The geograp­ McC!ure HE, Poonswad P, Greiner EC, hical distribution of animals. New York, Laird M. Haematozoa in the birds of eastern 1957 and southern Asia. St John's: Memorial University of Newfoundland, 1978 Desser SS, Bennett GF. The genera Leuco­ cytozoon, Haemoproteus, and Hepatocystis. Peirce MA. Distribution and host-parasite In: Kreier JP, Baker JR, eds. Parasitic Pro­ check-list of the haematozoa of birds in tozoa. New York et a!: Academic Press, Western Europe. J Nat Hist 1981; 15: 419-58 1993; 4: 273-307 van Riper III C. The impact of introduced Earle RA, Bastianello SS, Bennett GF, vectors and avian malaria on insular passeri­ Krecek RC. Histopathology and morphology form bird population in Hawaii. Bull Soc of the tissue stages of Haemoproteus colum­ Vector Ecol 1991; 16: 59-83 bae causing mortality in Columbiformes. Seed TM, Manwell RD. Plasmodia of birds. Avian Pathol 1993; 22: 67-80 In Kreier JP, ed. Parasitic Protozoa. New Gabaldon A, Ulloa G, Holoendemicity of York et a!: Academic Press, 1977; 3: 311-57 malaria: an avian model. Trans R Soc Trop Stone WB, Weber BL, Parks FJ. Morbidity Med Hyg 1980; 74: 501-7 and mortality of birds due to avian malaria. N Gabaldon A, Ulloa G, Zerpa N. Fallisia Y Fish and Game J 1971; 18: 62-3 (Plasmodioides) neotropicalis subgen. nov. Valkiiinas GA. Leucocytozoids (Haemospo­ sp. nov. from Venezuela. Parasitology 1985; ridia, Leucocytozoidae) as biological tags in 90: 217-25 populational investigations of birds. Parazi­ Graczyk TK, Cranfield MR, Skjoldager ML, tologia 1988; 22: 293-6 (in Russian) Shaw ML. An ELISA for detecting anti­ Valkiiinas G. Pathogenic influence of hae­ Plasmodium spp. antibodies in African black- mosporidians and trypanosomes on wild 113 birds in the field conditions: facts and hy­ potheses. Ekologija 1993a; 1: 4 7-60 Valkiunas G. The role of seasonal migrations in the distribution of Haemosporidia of birds in North Palaearctic. Ekologija 1993b; 2: 57- 67 Valkiunas GA, Sruoga AA, Paulauskas AP. On the geographical distribution of Leuco­ cytozoon simondi (Haemosporidia, Leuco­ cytozoidae). Parazitologia 1990; 24: 400-7 (in Russian) Vysotsky VG, Valkiunas GA, Population structure in the pied flycatcher (Ficedula hypoleuca) and the great tit (Parus major) according to the data on blood parasites. Russ

J Ornithol 1992; I : 85-95 (in Russian) White EM, Grciner EC, Bennett GF, Herman CM. Distribution of the hematozoa of Neo­ tropical birds. Rev Bioi Trop 1978: 26: 43- 102 Bull Scand Soc Parasitol 1996; 6 (2): 1 14-1 17

TREMATODE INFESTATION AS A FACTOR IN SHOREBIRD OVERSUMMERING: A CASE STUDY OF THE GREATER YELLOWLEGS (TRINGA MELANOLEUCA)

2 R. McNeil1 , M.T. Dfaz2, B. Casanova , A. Villeneuve3 and M. Thibault1 1 Departement de sciences biologiques, Universite de Montreal, C.P. 6128, Succursale Centre­ vine, Montreal, Quebec H3C 3J7, Canada; 2Instituto de Investigaciones en Biomedicina y Ciencias Aplicadas, Universidad de Oriente, Cumana, Sucre, Venezuela;3Departement de pathologie et microbiologie, Faculte de medecine veterinaire, Universite de Montreal, C.P. 5000, St-Hyacinthe, Quebec J2S 7C6, Canada

Abstract The relationship between digenean (see McNeil, 1970; McNeil et al, 1994). trematode infestation and oversumme­ Although most oversummering birds are ring on the winter range was explored in second-year individuals, the age as such Greater Yellowlegs (Tringa melano­ does not appear to be the causing factor leuca) in coastal Venezuela. Adults that (see McNeil et al, 1994). Indeed, indivi­ had recently arrived on the wintering duals of various species known to grounds were more infested with trema­ oversummer do migrate to the breeding todes than juveniles. By spring, this grounds and start breeding at the end of relationship changed and first-year birds their first year (McNeil et al, 1994). tended to contain more trematodes than Why do some birds oversummer while adults. The prevalence of trematodes others of the same age classes return to increased steadily from November to boreal regions and breed? In oversum­ Aprii-May. There was an inverse relati­ mering shorebirds, pre-migratory moult onship between fat loads and parasite and fattening either do not take place, or loads of birds collected by the end of the are delayed (see McNeil, I 970; McNeil vernal pre-migratory conditioning. et al, 1994). The relationship between Trematode parasitism appears to be an digenean trematode infestation, absence important factor causing oversummering or delay in premigratory conditioning in first-year birds, at least for the Greater and oversummering, first suggested by Yellowlegs. McNeil (1970), is tested here in Greater Yellowlegs (Tringa melanoleuca). Introduction Various hypotheses were proposed to Materials and methods explain oversummering (remaining on Greater Yellowlegs, obtained every wintering grounds during the boreal month from November 1988 to October summer) in boreal-breeding shorebirds 1989, and from January 1994 to August 115

1995, in coastal lagoons of northeastern gonimus ovatus and specimens of Mari­ Venezuela, were examined for digeneans trema, Stictodora, Odhneria, and Di­ (for more details, see McNeil et a!, plostomum were present only in juveni­ 1995). The fat content of birds was les. estimated based on a visual quantificati­ Taking into account non-infested (i.e. on (0 to 4) of fat deposits (McNeil, those having 0 parasite) and infested 1970). Adult (> 13 months old) and birds, the 26 adults collected in August, juvenile ( < 12-13 months old) birds were September and October shortly after distinguished based on plumage charac­ their arrival on the wintering ground had teristics and retention of bursa of Fabri­ an average trematode intensity (14.69) cius. significantly higher than that (0.25) of Results the 8 juveniles collected in September, October and November (Test of equality Except otherwise indicated, data of the means of two samples whose presented here are those collected in variances are unequal: t 1.9075, d.f. 1988-1 989. Of the 99 yellow legs (59 = = 25, P 0.034). In spring, the average adults and 40 juveniles) collected, 57.6% = parasite load of juveniles (68.69) col­ were infected with one to four digenean lected in March, April, May and June species. Eleven genera were found tended to be higher than that of adults (Table 1 ), hut only four were common (7 .00) collected during the same interval, both to adult and juvenile hosts. The but the difference was not significant (t trematode species diversity of juveniles, 1.6327, d.f. 12, P 0.064), although with 10 genera, was higher than that of = = = nearly so. In birds collected in 1994- adults (5 genera). Specimens of Prostho- 1995, infestation intensity for air sacs Table I. Prevalence and mean intensity of digenean trematodes infesting Greater Yellow­ l legs in nor herst ern Venezuela

Habitat Overall Mean intensity prevalence (range) Maritre1111t sp. Lower intestine 2.0 1.0 (I) Diplostom11111 sp. Lower intestine 1.0 1.0 (1) Stictodom sp. Intestine 6.1 130.0 (17-360) Mesorchi.1· denticulatus Lower intestine 19.2 22. 1 (1-194) Harrahium /l(tl/i Air sacs and body cavity 29.3 11.3 (1-61) Odhnerio sp. Intestinal tude and caeca 5.1 43.2 (1-140) Ta naisil1 ji·lilsi·hcllkoi Kidneys 10.1 8.8 (1-20) Prostho;.;onimus owl/us Bursa of 9.1 8.3 (2-20) Uvitellinu kni Air sacs and body cavity 3.0 13.0 (5-24) Parorchis a!'lllllhlis Cloaca 3.0 2.3 (1-4) PhilophthalmltS nol'lurnus Eyes, under nictitating 1.0 1.0 (1)

,�,��,,�w�'�"___ membrane ______..:.:�:..:.:..:;..;.;_..;.;_ -::-::- Number of examined hosts 99

Percentage of ho i nf d h helminths ______57.6 �l:: esl;.;:e;.;:;.;::.<.y. ...:....:..:.:=:..:...:.::...._ _ , 1 Prevalenee: Percent of host individuals infested by the particular trematode species. 2Mean intensity: Total number of individuals of a particular parasite species in a sample of a host species divided by lllllllher of infested individuals of the host species in the sample. 116

(all Cyclocoelidae: mainly Harrarium Discussion halli) was significantly higher in first­ The location of parasites as well as P year birds than in adults (F,,,, = 4.88, their number explain to some extent their < 0.05). The prevalence of digenean pathogenicity. Most parasites that infes­ infestation (adults and juveniles pooled ted Greater Yellowlegs were found in due to the small size of the sample) the intestine, air sacs and the body increased steadily from November, cavity. The detrimental effects of hel­ shortly after the arrival of juveniles, to minth infestation in birds are not well P April-May (r = 0.963, < 0.001). In known. However, in humans, pathoge­ fact, between mid-February and mid­ netic helminths depend upon the host for March, when yellowlegs had their hig­ nourishment, produce toxic substances hest premigratory fat load, there was a detrimental to the host, damage the host's significant decreasing exponential relati­ intestinal mucosa, cause intestinal ob­ (P onship < 0.00 1 ), adjusted by non struction, have irritative and inflammato­ linear least squares (see Jolicoeur, In ry actions, and sometimes undertake press), between fat loads and parasite b complex migrations through various loads (y = ae- x where a= 2.8224 and b = host's organs (Watson 1960). Many of 0.0239) (Fig. 1). these detrimental effects may apply to

4 •

3 • Ul Qj Ul Ul IV (j 2 .... IV LL.

1

20 40 60 80 100 120 140 Trematode intensity

Fig. 1. Decreasing exponential relationship between fat loads and trematode intensities b (y = ae- x) of Greater Yellow legs collected between 25 February and 17 March. migratory birds, as recognized by damage caused by trematodes, e.g. Wehrmann (1909). For a review of Cy clocoelum mutabile, which penetrate suspected detrimental effects of hel­ the intestine and enter the body cavity, minths on birds, see McNeil et al (1994). then penetrate the liver and, after a Interestingly, all helminths found in the period of development, leave the liver air sacs of yellowlegs, particularly and become established in the air sacs of Harrarium halli, pertained to the family the avian host where they mature, can be of Cyclocoelidae. Cyclocoelids often extremely severe (McLaughlin, 1977). have severe effects on their hosts It is therefore quite possible that, in (McLaughlin, 1977; Feizullaev, 1985; addition to causing enteritis, anemia and Howe & Scott, 1988). For example, the 117 death of some individuals, helminths Jolicoeur P. Unlinearized confidence limits may also prevent or delay normal moult for the statistical recovery of nonlinear and pre-migratory fattening in some relationships in biology. J Theor Bioi 1995; shorebirds on their wintering grounds, 217-24 and hence be an important factor respon­ McLaughlin JD. The migratory route of sible for their oversummering (McNeil, Cyclocoelum mutabile (Zeder) (Trematoda: 1970; McNeil et al, 1994, 1995). Diges­ Cyclocoelidae) in the American Coot, Fulica tive disturbances resulting from intesti­ americana (Gm.). Can J Zoo! 1977; 55: 274- nal helminth infestation are also expec­ 9 ted to result in similar effects. McNeil R. Hivernage et estivage d'oiseaux aquatiques nord-americains dans le nord-est Birds may develop some degree of du Venezuela (mue, accumulation de graisse, immunity to reinfection with particular capacite de vol et routes de migration). species of trematodes (for references, see Oiseau R F 0 1970; 40: 185-302 McNeil et a!, I 994, I 995). Partial immu­ McNeil R, Dfaz MT, Villeneuve A. The nity would explain, at least in part, (1) mystery of shorebird over-summering: a new why juvenile Greater Yellowlegs tended hypothesis. Ardea 1994; 82: 143-52 to be more highly infested with digene­ ans at the time of or prior to the normal McNeil R, Dfaz, MT, Casanova B, Villeneu­ ve A. Trematode parasitism as a possible spring migration period, (2) why adults factor in over-summering of Greater Yellow­ were also parasitized to some extent, and legs (Tringa melanoleuca). Ornitol Neotropi­ (3) why adults, which constitute the bulk cal 1995; 6: In press of those "scheduled" for migrating north, Watson JM. Medical helminthology. London: were less infested with trematodes in Bailliere Tindall and Cox, 1960 spite of the fact that the heavier feeding associated with fat accumulation almost Wehrmann (Nee Brodsky) S. Sur !'action certainly exposed them to greater risk of pathogene des Helminthes des oiseaux. Archv parasitic infestation. Parasitol l909; 13:204-38 Acknowled gem en ts Th is study was fi nanced by the Uni­ versidad de Oriente (IIBCA), Fundaci6n Gran Mariscal de Ayacucho, CONICIT (Venezuela), NSERC (Canada), Univer­ site de Montreal and Universidad de Oriente, through the collaboration agre­ ement between both universities. References Feizullaev NA. Pathogenic effect of tremato­ des of Cyclococloidea on the hosts. Parasito­ logia !9W1; 19: 248-50 (In Russian)

Hoeve .l, Scott ME. Ecological studies on Cyathocotyle lmshiensis (Digenea) and Sphaeridiotrema globulu.\· (Digenea), pos­ sible pathogens of dabbling ducks in southern Quebec . .l Wild! Dis 1988; 24 : 407-21 Bull Scand Soc Parasitol 1996; 6 (2): 118-130

ABSTRACTS OF SUBMITTED PAPERS ­ ORAL AND POSTER PRESENTATIONS

THE ACUARIOID NEMATODES periments suggested species in small (A CUARIOIDEA ) OF THE UPPER waders use amphipod intermediate hosts DIGESTIVE TRACT OF NEW and one species in a large wader () WORLD WADERS AND THEIR uses fiddler crabs. Twenty-three wader TRANSMISSION IN MARINE species lacked Skrjabinoclava sp. Host ENVIRONMENTS distributions seems related more to R.C. Anderson & P.L. Wong differences in foraging behaviour than Department of Zoology, College of Biologi­ physiological factors. cal Science, University of Guelph, Ontario, Eleven gizzard nematode species Canada occurred in 27 wader species. Dominant Objective: To identify the acuarioid hosts were usually larger waders (e.g. nematodes in the upper gut of waders in Godwits, Willets). Nevertheless wide the New World and to determine sites host ranges of species, even extending to and modes of transmission. Calidris spp., were striking and indi­ Material and methods: Approximately cated a lack of specificity and the possi­ 2000 waders consisting of 41 species bility of a diversity of intermediate collected in various parts of N. and S. hosts. Larvae in wintering birds indicates America were examined and nematodes transmission of at least five species were identified to species and stage. occurs on the Pacific and Gulf coasts of Host and geographic distributions were the U.S.A. and the Pacific and Atlantic determined. Presence of preadult stages coasts of South America. A species of was used to indicate sites of transmis­ Ancyracanthopis in willets reached the sion. Field data were supplemented by infective stage in fiddler crabs. transmission experiments. Results: Thirteen species of Skrjabino­ EPHEMERALITY IN FILARIOID clava occurred in the proventriculus of NEMATODES (EULIMDANA SPP.) 15 wader species. Each occurred in a FOUND SUBCUTANEOUSLY IN main host; six were found in only one CHARADRIIFORMS AND host species. Three occurred outside the TRANSMITTED BY LICE main host on only 1 to 3 occasions. Cheryl M. Bartlett Three species in small waders occurred Biology, University College of Cape Breton, more commonly outside the main hosts Sydney, Nova Scotia, Canada but usually in related waders. Larvae Objective: The study investigated the revealed transmission occurs in marine biology of a previously poorly under­ staging and wintering areas along Atlan­ stood group of filarioids in the genus tic and Pacific coasts of N. and S. Eulimdana occurring in charadriiform America and the Gulf of Mexico. Ex- birds. 119

Materials and IIH'Iho!h: r·-k · !op;-. y ilJHI parasites (lice) that might otherwise parasitological cxml!llhtl l"��'• \\T il' rar· ingest lethally high numbers of microfi­ ried out on 3S SJh'< w·. ol , h;ttil!htti JWrw:. ol Fulinulono. 17 FAMILY PHILOPHTHALMIDAE species of httd:. Wt't•· i nfect ed TRA V ASSOS, 1918 IN THE AMERI­ (Charadrius hiulli lllu, ( 'hlulunius nigcr, CAN OYSTERCATCHER, HAEMA­ Larus pi pi \I'll!/, Stn 1111 ltinmdo, Recur­ TOPUS PALLIA TUS IN THE NORTH virostm umtrinnw, i\ 1 t'lltlltil inl<'rpres, - EAST COASTAL OF VENEZUELA Calidris oi/Ju, (' 1//f'illu, ( '. hainlii, C Marcos Tulio Dfaz and Susana Ramos himaniOJIIIS, ( · J.lll,\i/111, ( 'otoptrophorus Instituto de Investigaciones Biomedicas y semipollllutus. Unw.1u fr·rloo, Numenius Ciencias Aplicadas , Universidad de Oriente, phacoJIIIS, l'hllhll Of ills lo/Jatlls, P. tri­ Cumami, Estado Sucre, Venezuel co/or, r, ingo llll'ltlnoll'l/C(/). Adult Objective: The purpose of the work was worms \H'CIIIIl'd in t he twck region and to study the digenean trematode infesta­ microfllari;w 111 tiH' skirL llowever, the Charadr­ comhi nat ion of adult worms and micro­ tion in the shorebirds families iidae , Scolopacidae and Haematopodi­ filariae was fotiiHI i n only 6 of the 116 dae infected adult birds but in 9 of the 18 on North - east coastal Venezuela. infected jnvcnill:s. Birds not infected Material and Methods: Birds were included ( '!tarwlrius voc(ferus, C semi­ killed with a shotgun and examined for palmatus. 1'/uvia/is apricaria, P. squa­ parasites within 2 h of death. We exam­ tarola, /,oms argentatus, L califo rnicus, ined living specimens of adults and L dl'laworl'nsis, L marinus, Bartramia whole mounts of heat - killed, AFA - longicwulo, ( 'a/idris canutus, C mari­ fixed specimens stained with Semichon's tima, C. 11/tlllri, C. mclanotos, C minu­ aceto - carmine and mounted in moun­ tilla, ( ;a/linuuo gallinago, Numenius tec. Drawings were made with the aid of americm111S, Tr inga f7avipes and T. a camera lucida. totanus. Results: During a systematic investiga­ Discussion: Course of infection in birds tion on the trematode fauna of shorebirds is suggested to be: (I) acquisition of families Charadriidae , Scolopacidae infections (via lice vectors) as neonates; and Haematopodidae on coastal Vene­ (2) rapid maturation of worms to sexual zuela, the small intestine of four Haema­ maturity; (3) short, intense period of topus palliatus were examined and production of microfilariae; (4) early found to be infected with parasites death (=ephemerality) of adult worms belonging to the genus Skrjabinovermis and their complete resorption by the Belopol'skaia, 1954. The parasites found host; and (5) long term survival of mi­ in this study can be separated from the crofilariae in the skin. Ephemerality is hereto identified species of the genus, highly unusual among filarioid nema­ Skrjabinovermis vesiculata Belopol­ todes, as is the combination of louse 'skaia, 1954, on the basis of the body transmission and skin-inhabiting micro­ which is completely spinose, a head with filariae. Ephemerality curtails microfi­ a double crown of small spines, presence larial production and may be an adapta­ of pre - pharynx, cirrus spinose and the tion to transmission by permanent ecto- 120 smaller size of the body , ovary and eggs. Conclusion: The results indicate /. uriae Conclusion: As a result of these com­ role in the circulation of the Tuleny virus parative studies, the present material is in the natural foci of the bird colonies on considered to represent a new species the seashore of the European Zapolarja. and is named Skrjabinovermis hae­ The discovery of antibodies to viruses of matopi. group B and Uukuniemy in the bird's blood serums is evidence of the bird's role in the circulation of the above­ TICKS IXODES URIAE AND THEIR mentioned viruses on the studied terri­ PARTICIPATION IN CIRCULA­ tory. The discovery of antihemaglutinins TION OF ARBOVIRUSES IN to TBE in the guillemots blood serum BREEDING COLONIES ON THE allow to suppose the circulation of this BARENTS SEA COAST virus among the sea colonial birds in the Galina Efremova and Alexander Gembitzky high latitudes. Institute of Zoology, Belarus Academy of Sciences, Belarus GULLS (LARIDAE) IN ICELAND Objective: The complex parasitological AS FINAL HOSTS FOR DIGENEAN and virological investigation of the birds TREMATODES in the breeding colony of Barents sea * * Matthfas Eydai , Brynja Gunnlaugsd6ttir & coast were conducted in 1973-1974. ** Droplaug 6lafsd6ttir * Material and methods: In the bird Institute for Experimental Pathology, Uni­ colonies on the seashore of the islands versity of Iceland, Keldur, Reykjavik, Ice­ ** more than 30.000 ticks Ixodes uriae land, Marine Research Institute, Reykjavik, White, 1852 in all developmental stages Iceland were collected. Eighty-one samples of Objective: To study the helminth fauna blood serum of Uria aalge and 174 of gulls in Iceland. Here we present samples from Rissa tridactyla have been some preliminary results on the digenean examined by virological investigation. trematodes found in the study. The virological investigations were Material and methods: The intestines carried out on 2-3 days old white mice of 56 gulls (14 Larus marinus, 17 Larus by means of intrabrain infection of 10% hyperboreus, three Larus argentatus, material suspension. three Larus glaucoides and 19 migratory Results: The spreading of the /. uriae on Larus fu scus) killed in SW- and W­ the Kolsky peninsula and on the Barents Iceland in 1993 and 1994 were examined Sea islands coincides with the natural for the presence of helminth parasites. habitat of auks. On the Murmansk's Results: One or more species of digene­ seashores and the Barents sea islands the ans were found in 42 (75%) of the gulls. main hosts of ticks are guillemots and The following digeneans were identified: kittiwakes. Virologists have isolated 8 strains of Tuleny viruses form 1.735 Cryptocotyle lingua was found in all ticks. Antihemaglutinins to the Tuleny the host species examined; Larus mari­ and Uukuniemy viruses from the bird's nus (prevalence 71%) L. hyperboreus blood serum were discovered. In addi­ (35%), L. argentatus (67% ), L. glaucoi­ tion antibodies to the tick-borne en­ des (33%) and L. fu scus (47%). The cephalitis (TBE) were found in the number of C. lingua ranged from 1-163 guillemot's blood serum. per gull. 121

Micn,ph;dluLtc lni!nd 111 all Sea food fish and molluscs with trema­ the hos t '•I ., . , • �•!!Wflnl, 1<11/IS todcs. marinus I (HrvuktH ' id' I h\'fll'r Material and methods: Original and boreus ( /h'.l 1. I 1 ! I!Hl'/) ,}, /, literature data on the seabird, fish and glaucnit!l'.l 1 '"' 1 I I 'X, ). mollusc trematodes from the Black Sea The Illllllllt•i ''' IIOili I were summarised. 2370 Jll'l ������ Results: In the Black Sea region the lfi111o 1fhlu •; pp l11111!d unly in marine and coastal birds have 135 tre­ Lams h\'/'�'� "• 11 qn vnkm t' 7')%) matode species. Only 23 species use the and /.a 111 1 w 1. I !iO' ; l t!l lllllllhers marine fish as the second intermediate rangi ll)'. fJtol!l l I i!l hosts. Most frequently metacercariae of

Twt l not tdt'lllil h'' I "I "''�' it·�; were the trematode genera Cryptocotyle, recovc11'd lwm a lnws /IISi'/1.1'. Galactosomum, Cardiocephalus and Knipowitschetrema occur in the Black Blotul llt!J,,.,, lwhll!,! ' llJV to llw genus Sea fish. Omirllo/!!lltlll 111 w,.,,. tt•ruvc�t·d during rnacnJ�it llJlh •nn!!lilllt�!l of tht· intesti- Most of them are pathogenic for nal wall of tin lmll.\ /lw 11.1 i nd i v idu- their fish hosts. Some of them have the als. high prevalence and intensity indices. Com.·lusluus: TIH''>t' JHCIIJninary results Mullets, gobies, smelts, flounder, turbot and some other fish are the most in­ show that v.ulb 111 J , l'lnnd st·rve as final vaded. A discrepancy between quantity hosts lor 'W W!i!ldw. r· twans. The digene­ of species of adult trematodes found in ans aht•ady tdvntd ll·d ill the present marine and coastal birds and findings of study compkk then hit' c yc les through their metacercarial forms is revealed. di fferen t inlcflllnltah' llll.�ts which occur Five trematode species use the molluscs in the inl!'rt ulal m m tlw �;nblittoral zone. as the second intermediate hosts. Only Prevalence dlilcH'IH'�"S nf digeneans one species, Parvatrema duboisi is betwt�ell gtlll spt't it.' '; pwbab ly reflect pathogenic for its host, the mussel different lecdinp, habits and different Mytilus galloprovincialis. It causes the habitat selection of tilt� gull species formation of pearls and can decrease the examined. reproductive potential of the mussels. All the seabird trematodes can be THE ROLE OF BLACK SEA classified in to two ecological groups. MARINE AND COASTAL BIRDS IN Trematodes of the first group inhabit the INFECTIONS OF FISH AND native coastal birds, their life cycles are MOLLUSCS WITJ I TREMATODES linked with native hydrobionts and their Albina Gaevskaja & Vladimir Machkevsky occurrence along the Black Sea coast is Institute of Biology of the Southern Seas, more or less stable. Trematodes of the Sevastopol, Ukraine second group are the parasites of sea­ birds having the seasonal migrations and Objective: The purpose of this study appearing in the Black Sea in autumn. was to analyse the role of marine and Prevalence and intensity indices of such coastal birds in infection of the Black species have irregular character. 122

GUT PARASITE LOAD AND DIET species which infect the birds. The birds OF WADERS: METHODS AND fitness also has an indirect impact. We FIRST RESULTS show the need for further studies about eggs identification, parasites patho­ Sophie Le Drean-Quenec'hdu* & John Goss­ genicity and biology to allow to distin­ Custard**. guish causes and effects of parasite load. *Laboratoire d'Evolution des Systemes Naturels et Modifies, Universite de Rennes I, France. Some questions may be asked about the **Institute of Terrestrial Ecology, Furzebrook impact of bird parasites on the interme­ Research Station, Wareham, Dorset, United diate host population, especially shell­ Kingdom. fish for human consumption. Objective: We report a study of the gut parasite load of Oystercatchers THE ROLE OF DIFFERENT (Haematopus ostralegus ) from the Exe GAMMARID COMMUNITIES IN estuary (United Kingdom) in order to TRANSMISSION OF POLYMOR­ examine a possible relation with their PHUS MINUTUS (ACANTHOCE­ diet. The reason for the choice of both PHALA) TO EIDERS the wader and the study site is the im­ portant background on diet and feeding Jukka T. Lehtonen* & Martti Hario** Department of Ecology and Systematics, behaviour available for this site. Division of Population Biology, University Methods: We detail the methods to of Helsinki, Finland. allow a standardisation with other stud­ ** Finnish Game and Fisheries Research ies. The method used is coprology, Institute, P.O. Box 202, FIN-005 1 Helsinki, which is the research of parasite eggs in Finland waders droppings by flotation. Objective: The most common acan­ Results: We describe the eggs found in thocephala species in eiders (Somateria the faeces, principally Trematoda Psi­ mollissima) in the study area at Soder­ lostomum brevicolle, Meiogymnophallus skar, Gulf of Finland, is Polymorphus minutus and Nematoda Capillaria sp. minutus. Its cystacanth is transmitted to eggs. We show the difference in the eiders by amphipods of the genus Gam­ parasite load between the birds that feed marus. In this study the dynamics of P. on different prey species (mussels Myti­ minutus transmission to eiders in differ­ lus edulis, cockles Cerastoderma edule, ent gammarid communities were quanti­ other bivalves, Lumbricidae), between fied. birds of different fitness, and between Material and methods: In 1989-93 months. The birds that are most para­ gammarids were collected in the study sitised are those that feed not only on area from two main follow-up sites, mussels or on cockles, but also on Lum­ further divided into five "habitat" types. bricidae during high tide periods, that is The main types were sea-water ponds to say birds with the lowest fitness. and the littoral Fucus-zone. The sam­ Discussion: We discuss the advantages, pling periods were related to the differ­ drawbacks and the interpretation of the ent phases of the eider brood rearing methods. We interpret the results as period. The stability of the gammarid indicators of the bird's physiological and communities was estimated by means of immunity state and of the state of the similarity indices. environment where they feed. We con­ Results: The total prevalence of cysta­ clude that the diet influences the parasite canths paralleled the peak abundance of 123 ducklings. 'llw !'�•'Vt!kiH

Gamnuntl.l' ��� �·,mu il 11 1ilfim1s, (1. tion of the seabird fauna as well as the zaddachi and l, dw /•1'1!1 The JHCVa· space- and temporal distribution of the lene e also d!l ki rd l 11 Hll Ill I!' .•,;unpl ing seabird species in the area. site to anutlwt , !lw !!Will! J llt'Valence Seventeen seabird species overwin­ being hi/'Jw•.! 111 Ill•· •.hnll�>wlt! toml zone. ter in Sevastopol's bays. Distribution of Howcw1, llw bt·t wrn1 \Till vari at ion of the bird species over the bays depended preva l<· nn· lVII'• lnglw•.! 11 1 llw ;wmi · open on the depth of the water, presence of rock ptllld, whtt h nh11 was the least food, cover and the weather conditions. stable sl!l!lpluw ·<�I•· The main factor regulating the distribu­ Condusiun: /' llll!lli/ln ran rnax muze tion of the seabirds in the aquatorium of its tr:tll!·.tnh;dtHI 11 1 tlw dl'linitivc host by Sevastopol aquatory was the air tem­ means of 1'\m l llllllllfl.. lt alsu has to perature. adapt lu tlw :.t:!Pi!lllill dynamics of the internwdw!t· llo:;l The d i fferent preva­ EXPERIMENTAL INFESTATION lencL•s IHtllt till!' f.llllllll:l rid species to OF SEA-GULLS BY EYE-FLUKES anot lwr \W ir' lilll.'il ly explai ned by differ­ FROM THE THREE-SPINED ent life cyrh·•; nl SJWt' ll'S. STICKLEBACK Instable st·a watn ponds can be an Jolanta Morozinska-Gogol & Jerzy Rokicki imrHnlant l;wlor n•gul ating the popula­ Department of Invertebrate Zoology, Univer­ tion dy n a m i c:; of J>. minutus. When the sity of Gdansk, Gdynia, Poland wea t hn is stdtahle, seawater ponds can accunHJlatc great quantities of gam­ Birds from the families Laridae and Anatidae are final hosts of Digenea from marids , which leads great numbers of feed i ng cidns to excrete faeces contain­ the family Diplostomidae. Adult forms ing acanthou�phalan eggs. of Diplostomum spp. occur in the diges­ tive tract of fish-eating birds. Metacer­ cariae live in eyes (generally in eye-lens) MONJTOIU NG OF OVERWINTER­ of many species of fish. Eight young sea­ ING SEABmDS IN SEVASTOPOL'S gulls Larus ridibundus were infected by BAYS eye-flukes from the eyes of three-spined Vladimir Machkevsky &. Roman Mach­ stickleback Gasterosteus aculeatus. Five kevsky, sea-gulls were infected by flukes from Institute of Biology of the Southern Seas, eye-lens and three by flukes from vitre­ Sevastopol, Ukraine ous body of eyes. After few days birds The aquatorium of Sevastopol is formed were euthanasied by ether and the intes­ by numerous bays. Fifteen years ago the tines were studied. ecological situation of this area was In the intestines of experimentally destabilised as a great breakwater, infected birds (by eye-lens) adult stages crossing the main harbour was built. of Diplostomum sp. were found. On the Since then the ecosystem has changed basis of the metric data and the mor­ and new seabird speeies have appeared. phology of adults, parasites were identi­ fied as Diplostomum spathaceum. 124

NEMATODE INFECTIONS IN ICE-. The following nematodes were LANDIC SEABIRDS found in the birds: (L3 Droplaug 6Iafsd6ttir, Kristjan Lilliendahl & and L4 stage), Pseudoterranova decipi­ J6n S6lmundsson ens, Hysterothylacium aduncum, Hys­ Marine Research Institute, Reykjavik, terothylacium sp., Contracaecum oscu­ Iceland latum, Contracaecum variegatum, Cu­ Objective: The aim of the study was to cullanus sp., Stegophorus stellaepolaris, investigate the nematode fauna of Ice­ Seuratia shipleyi, Streptocara crassi­ landic seabirds with emphasis on its cauda, S. californica and Paracuaria connection to the bird' s diet. adunca. Material and methods: Samples of 180 No geographical differences m fulmars (Fulmarus glacialis), 261 guil­ nematode infections were observed but lemots (Uria aalge), 73 Briinnich's infections varied between bird species. guillemots ( Uria lomvia), 198 puffins Young fulmars harboured similar nema­ (Fraterculaarcti ca), 154 razorbills (Alca tode burdens as did older individuals but torda) and 193 kittiwakes (Rissa tridac­ nematode infections in young birds of tyla) were collected on the birds' feeding other species were insignificant. grounds off Litrabjarg (W-Iceland), Prevalence (P) and mean intensity Horn (NW-Iceland), Grfmsey (N­ (MI) of A. simplex were highest in Iceland), Skrudur (E-Iceland) and Vest­ fulmars (P=33,3%, MI=5,4) but ranged mannaeyjar (S-Iceland) in June to in other bird species from occurring in August 1994 or, in case of young birds, one out of 198 puffins to P= 15, 1% and from the nests. Stomach contents of all MI= 1,2 in Briinnich' s guillemots. samples were investigated for diet and Contracaecum variegatum was most parasites. Sixty-five kittiwakes, 31 frequent in razorbills (P=8,5%; MI=2,0). razorbills, 89 guillemots, 54 Briinnich' s It was less frequent in other bird species guillemots and 99 puffins, all adult birds, and was absent in puffins. were analyzed further for nematode infection under the gizzard lining. Stegophorus stellaepolaris was found in all bird species but its infection Results: Puffins, Guillemots, Razorbills rates were by far the highest in fulmars and Kittiwakes feed mainly on capelin (P=91,1% , MI=95,8). Infection values of (Mallotus villosus) off the North-Coast S. stellaepolaris in other species ranged but on sand-eels (Ammodytes spp.) off from P=2,5% and MI=1,4 in puffins to the West, South and the East Coasts. P=28,8% and MI=18,0 in Briinnich's Euphausids and small crustaceans are guillemots. also prominent in the diet of these birds. Briinnich' s guillemot, which is only Seuratia shipleyi was found in distributed off the North Coast flies long puffins (P=4,0%, MI=l,O) and fulmars distances from the coastline to feed and (P=4,4%, MI=1,4) but in only one the diet consists mainly of large capelin, kittiwake and razorbill, respectively. sand-eels, euphausids and pelagic gam­ Streptocara crassicauda was found marids. Fulmars feed on same diet as the under the gizzard lining in one guil­ other species but fish carcass and liver lemot. Streptocara californica occurred thrown to sea from fishing boats seem to under the gizzard lining in all bird spe­ be a considerable part of their diet. cies but was only frequent in guillemots 125

(P=l5 ,71/r, , f\11 I PATHOLOGICAL STUDIES ON (P=2 1 M I I. ' l COMMON EIDERS FROM O P111'111'11dl li! lli'!jiH'IItly SKERJAFJ RDUR, SW-ICELAND. observed 1111d•'! t!" lmttl).', in Sigurour Siguroarson*, Slavko Helgi Bam­ kittiwakt·�,, (! • cl \) httl was bir**, Karl Skfrnisson** and Arn6r J:>6rir found in wd tHH !illrlll• l! i!llll Briln Sigfusson*** nich's l',!lllkmPI '' ',pr• 11 lv *Central Veterinary Laboratory, Keldur, Iceland. Condusinn: 11111{'/n , 1'. de­ '\ Ill 11 ** Institute for Experimental Pathology, cipil'/1.1 , llntll oiln l. t. 111111 :. pp , ( '. oscu­ Keldur, University of Iceland, la!ti/11 and r '11• '•PP an· not true ***Icelandic Institute of Natural History, bird p:u iPill•''• i\ll/l!lh,l\ Mmp!t• 1, how­ Reykjavik, Iceland. lW t· f, ;;,•ctn to \ ill V! Vt' t111 sonn.'. time in Objective: Unusual mortality is occa­ birds and di'\Tinp to tlw lnurth stage. sionally observed in local population of 1\nisoh i.l \llltf'l'' ' h p1 o l>ahly mainly the common eider (Somateria mollis­ trans!IHII!'d lu ht�th by ingc,st ion of sima) in Iceland. Sometimes the causes c;qwlin iiiHI c,;md ,.,.h lmt hi gh infections are obvious (oil spills, fat contamination in ft thttat lllP:.t likdy achieved by :11 1' or the renal coccidian Eimeria somate­ in).!J'Siwn ol lt•,IJ liiii'HSs a1;d liver thrown riae) but most often reasons for these t o !lw ;,,·a ftulll lishing boats. Large deaths remain unknown. In 1993 we in fect it Ht!• 1 d ,)'.. lft•l!at·polaris in fulmars began an extensive study on the eider may ;!1:"' lw t'OIIIH'rted to their ingestion population of Skerjafji:irour, SW -Iceland. of fishra n·as;;, I .ow worm burdens of C. Here we present the results from the varh·gotum and S. stellaepolaris in puffins twlkatc low importance of sand­ pathological examination of these birds. eels (1\m/111)(/ytt·s spp.), puffin's main Material and methods: On four sam­ food ill' tlt, for transmission of these pling dates (Feb., May, June, Nov.) 78 m�matod1'S, Small body size and thus less eiders (66 adults, 12 immature) were food intakt' may fu rthermore explain shot. Ten females and ten males were generally lowt�r nemat ode burdens in sampled each time except in November puffins, compa red to the other bird only eight males. Birds were obducted, species. l'amclltll'ia rulunca seems to macroscopic pathological changes de­ have pn:dilL·ction for gu lls explaining the scribed and samples taken for micro­ low infections in other birds than kitti­ scopic studies. wakes. Results. Parasite induced lesions were The different nematode infections found in the digestive tract of all birds between bird species arc undoubtedly varying from mild diffuse hyperaemia of results of different diet hut may also be the mucosa to intense thickenings of the due to host specification at some degree intestinal wall. Nodules in the intestinal or the birds may have brought nematodes wall where proboscis of acantocephalans from different wintering grounds. Fur­ had previously been embedded were ther studies on the birds' diet will hope­ seen in almost all birds. In 9% of the fully lead to better knowledge of the cases acantocephalans had partly pene­ intermediate hosts. Any indications on trated the intestinal wall. These lesions relationship between nematodes and the were most prominent in February and birds' diet must, however, be followed by May. direct investigation on the suspected Pathological changes were seen in intermediate hosts. the heart of 35% of the birds. Prominent 126 changes were greyish foci in the epicar­ PARASTIES AND ECOLOGY OF dium. Thickenings of the ventricle wall THE COMMON EIDER IN were also seen in 15% of birds. Micro­ ICELAND scopic examination revealed epicarditis Karl Skfrnisson* & Aki Armann J6nsson** and myocarditis with infiltration of *Institute for Experimental Pathology, lymphoreticular cells. Keldur, University of Iceland, Reykjavik, Small grey nodular spots were seen Iceland, in diffusely enlarged kidneys in 9% of **Wildlife Management Institute, Akureyri, the birds. Microscopical examination Iceland revealed nephrosis of the renal tubules Objective: The aim was to study the and infiltration of lymphoreticular cells. parasites of the common eider (Soma­ feria mollissima) in Skerjafjorour, SW­ White nodules were found in the Iceland including seasonal and sex­ liver of 10% of the birds. Adenoma was related differences in parasite load and found in the bile duct of the liver in one relate the findings to the life-strategies bird. of the eiders. This study is a part of an The pancreas of one bird was en­ extensive project on the condition of larged. Macroscopically whitish nodular eiders which started in 1993. proliferations were observed. Micro­ Material and methods: Altogether 78 scopical examination revealed hyperae­ eiders (66 adults, 12 immature) were mia and focal haemorrhagiae of the shot on four different sampling dates in parenchyme. Cystadenoma was found in 1993 (10 February, before and after the the pancreatic duct of one bird. Ade­ incubation period on 11 May and 24 noma was found in the testis of one June respectively, and 2 November). Ten male. The spleen of two birds was ab­ females and ten males were collected normally small and atrophic indicating except in November when eight males exhaustion of the immune system. were sampled. Blood smears were ex­ Reticuloendotheliosis was com- amined and ecto- and endoparasites monly observed in the sections from the searched for. Metazoan parasites found hearth, kidney, liver and ovary. In 2 birds either counted or numbers estimated focal discoloration of heart muscle was from samples. Dr. G. Valkiunas exam­ observed and microscopically hyaline ined the blood smears for hematozoans. degeneration was found, similar to white Identifications of helminths were further muscle disease in lambs. Skeletal muscle checked at CAB International Institute of degeneration and lipofuchsin pigmenta­ Parasitology, St Albans, UK. tion was frequently observed. Results: No blood parasites were found. Conclusion: Diverse pathological le­ Two ectoparasites; a feather lice be­ sions were found. Most prominent longing to the genus Anatoecus and the changes was a chronical granulomatous flea Ceratophyllus garei were found. enteritis. Disseminated reticuloendothe­ The only protozoan observed was an liosis observed in several organs suggest enteric Eimeria sp. Digeneans detected viral infections. Skeletal muscle degen­ in intestines were Gymnophallus cf. eration and lipofuchsin pigmentation are somateriae, Microphallus pygmeaus and probably related to nutritional imbalance vinseniella cf. propinqua. In heavy and seasonal starvation. Benign tumours infections these species were also found (adenoma and cyst adenoma) were in the ceca. Psilostomum cf. brevicolle incidental findings. 127

n and a n ltn1• ,, tlltr' I V flltliHI in life-cycles of the parasites found, prey inlt"•l l l!! , hilrat!rii the 1 , I , selection of the birds and seasonal

./(Jimls \\'.1', • hh! lolllul m the ceca. changes in the food intake. i Cutull ot•n lW • ' o!, l' llll!'d n the In this study 20 parasitic species ·, hut kw ceca ul liut·,l nd•·l individuals were recorded for the first time in Ice­ in were :; Pnl!'i!IJH'\ 11ho I!H!Ild the intes­ land and two species are probably new nes ;iftd htll c·ll l·abt kii. ti The kidney host records. fl uke Rr'lll• o/11 .\umatrriocwas occasion­ ally fo und 111 IIH' k idneys . Gymnophallus cf. '1'• '11/i·rlot'IIS occurred in the gall SEASONAL CHANGES OF THE hladdl·t ol most birds. At least nine FOOD COMPOSITION AND CON­ c,;e.stodt·s ( Fimhriarioides intermedia, DITION OF THE COMMON EIDER r.a/t'l lf!0/'1/S le res, Dilepididae sp., IN ICELAND i i D cmnotacn a fa llax and Microso­ Karl Skfrnisson*, Aki A. J6nsson**, Arn6r P. lllllUIIIflllls spp.) were detected in the Sigfusson*** & Sigurour Siguroarson**** intestines. Nematodes were most often * Institute for Experimental Pathology, found in the gizzard (Amidostomum Keldur, University of Iceland, anseris, T. fissispina, Echinuria unci­ ** Wildlife Management Institute, Akureyri, nata, Streptocara crassicauda and S. Iceland, dogieli) but also in the proventriculus *** Icelandic Institute of Natural History, (Tetrameres somateriae), intestines Reykjavik, Iceland, (Capillaria sp.) or both in intestines and **** Central Veterinary Laboratory, Keldur, ceca (Capillaria nyrocinarium). Three Iceland. acantocephalans (Prqfllicollis botulus, Objective: In 1993 an extensive study Polymorphus minutus and Corynosoma was started on the condition and some strumosum) were found in the intestines. ecological aspects of the common eider For general, seasonal and sex-related Somateria molissima in Skerjafjorour, comparisons prevalence and mean inten­ SW-Iceland. Here we present some sity of each parasite were done. These preliminary results on the food compo­ results were related to the life-cycles of sition and the condition of the birds. the parasites. Furthermore to the prey Material and methods: Altogether 78 selection and the total food intake, eiders (66 adults, 12 immature) were habitat utilisation and the life-cycle of shot on four different sampling dates in the common ciders. 1993; 10 February, 11 May, 24 June and Parasite induced pathological 2 November. Ten females and ten males changes were rnost often observed in the were sampled at these dates except in different parts of the alimentary canal. November, when eight males were Pathological changes were related to the sampled. Birds were weighed and the degree of invasion and the parasitic amount of subcutaneous and intrab­ species occurring. dominal fat was assessed macroscopi­ cally on a scale from 1 to 6. The food in Conclusions: Eiders arc hosts for nu­ the gullet and gizzard was analysed and merous parasitic species which quite the prey species identified by compari­ often occur in very high numbers. son with undamaged samples of poten­ Marked seasonal and sex-related changes tial prey species from the study area. For in parasitic load were observed for most semi-quantitative comparisons each of the parasites. Prevalence and intensity gizzard content got a score of altogether changes seem to be closely related to the 128

100 food-units, which were divided invertebrates which are selected on proportionally according to the volume rocky sublittorate substrate. Marked of each prey, estimated macroscopically. seasonal and sex-related changes in food Results: Although seasonal weight selection were observed. Several para­ changes were observed in both sexes sites of the eiders complete their life­ most marked changes in weight and cycle in intermediate hosts which are an condition were seen in the females important food source for the eiders in before and after the breeding period the area. Many of these parasites are when the mean body weight was reduced pathogenic and cause severe damage, by 1/3. especially when infections are massive. The amount consumed of these interme­ Altogether 35 prey species were diate hosts can therefore easily affect the identified. Bivalves were the most im­ condition and reproductive success of portant food source, 38.8% of the diet the females. (of which Mytilus edulis formed 28.2%). Gastropods were 19.1%, crustaceans 16.8% and Stylea rustica 1.5%. Bread, MORTALITY ASSOCIATED WITH fed to the eiders at Lake Tj ornin in the RENAL AND ENTERIC COCCI­ centre of Reykjavik, as well as waste DIOSIS IN JUVENILE COMMON consumed at sewage outlets in the study EIDERS IN ICELAND area was also an important food source, Karl Skfrnisson*, Sigurour Siguroarson**, i.e. 6.3% of the diet. Sand and grit Slavko H. Bambir* & Arn6r P. Sigfusson*** formed 13.1 %. Vegetable matter (algae, *Institute for Experimental Pathology, moss and grass fragments) were 3.7% of Keldur, University of Iceland, Iceland the diet and were found in 9% of the **Central Veterinary Laboratory, Keldur, birds but it is regarded to be of no sig­ Iceland nificance as food. Predominant food *** Icelandic Institute of Natural History, groups varied markedly by seasons. Reykjavik, Iceland Different prey selection of males and Objective: The cause of unusual mor­ females was most prominent on 11 May tality observed in late June 1993 among and 24 June when the males consumed newly hatched ducklings of the common significantly more bivalves than the eider (Somateria mollissima) in a colony females. In June, however, the females of approximately 600 breeding eiders at consumed significantly more gastropods Bfldudalur, W-Iceland was studied. than the males. Materials and methods: Fourteen Conclusions: Females gain weight due ducklings were autopsied and bacteriolo­ to increased food consumption in late gical, parasitological, pathological and winter when the food intake is increased histopathological examinations were up to three times the normal amount in done. order to lay down fat reserves for the Results: Routine bacteriological tests incubation period. During this time the performed were negative. Parasitological males actively defend an area around examinations revealed infection with an their mates. The marked weight loss of enteric Eimeria sp. in most of the duck­ females from 11 May to 26 June is due lings. Slight to moderate intestinal to starvation during incubation. Eiders infections by the trematodes Gymno­ are opportunistic feeders which are able phallus somateriae, Microphallus pyg­ to forage on a wide variety of benthic meus, Catatropis verrucosa, the cestode 129

Til E RHINONYSSID MITES (GAMASJNA : RHINONYSSIDAE) OF

wen· '" IIH ;�,,, I•. IIJl )');, SOME MARINE AND COASTAL A pt, •ntlll•'nl lll'il 111 all BIRDS duckiHII' ld dncys Maria Stanyukovich whkh Zoological Institute of Russian Academy of yell! l\\ I ·, I! •;j ! ll 'ill •, ('()f) ' Sciences, St Petersburg, Russia n d t a i r li!;!k , IVii lals Objective: The purpose of the study was and hill''' t!lilnl n! th• h'll;d n•t·ndian to examine the fauna of the rhinonyssid J•:ifllr'!/d mites of some marine and coastal birds (Anseriformes, Charadriiformes) of

Sli/11(/{t'i ill I'· d','>II!!Hd (w 1!'\fJ! liiSibit� Russia and adjacent countries. The ana­ I lysis of species diversity of rhynonys­ fOJ !lw dqth· " ' t h. dw t. In!)''· IIJ:;topa · sids, parasiting in the nasal cavities, tholt'l'.l<,If •·\nOlllll!IIP!I " ' ilw tnlc:;l i nt:s trachea and bronchi of birds, will de­ I f!,"d!ll!l lun and shown! l11 1, velop a basis of study of ecology of lll'<'l tli>f', ,,f \Jilt uldt' ill ill)' lhal llw l' lllt> rhinonyssids and their interrelations with ri1· Filllf'l t!l ·.p llllflll '" .,. h;� 'ontrih· their bird hosts; it will also give addi­ utl'd lu llw tkntlt nl !!11• " ' tlw ln11ls. tional information on bird evolution. Condusiou.;,: lt i'i '•.•wtdctnl that the Material and methods: In this study we

pri111ary ,·;tw.,· " ' Ill,· Ptlllll>'ilk was an use rhynonyssid mites collected from

envirollllll'lllal ill ' Hh·lll 111 llw fjord Anatidae, Charadriidae, Sternidae, Alci­ adjacen t lt> t l w ln,·,•dtill' , '""''Y which dae and Laridae birds from collections of reduced tltc :tvatlahk '"'111 i!lld ca used the Zoological Institute of Russian Academy of Sciences, St Petersburg and starvation :tlllOI!p, tlw wwlv ha tched the Okskii State Biosphere Nature Re­ duck I i ngs . serve. Mites in a liquid of For-Berlese Two WcTk:. pt tPt lt• the ttnusual were studied under the light microscope. mort al it y lH')')lll a L!l}'c •,, .11,• washing of Results: In the nasal cavities of 21 gravel in a riwrlwd , lu•,,· lP lilt� fjord. species of birds from the families Anati­ Du ring this ti11w a:, 1wll :1:; PilL� week dae, Charadriidae, Sternidae and Lari­ after the llH>rlalitv :,lilfl l'd 111:tsscs of mud dae, the following species of rhinonys­ were conllnw>ltsly 'nnicd IJy t h is river to sids parasite were found: Rhinonyssus

the fj o rd . The :�cnlnHdnling nHid-layer levinseni, R. rhinolethrum, R. minutus, on t he sea lwd was 11p tu cm thick at R. bregetovae, R. shcherbinini, R, cale­ the boll o 111 of !Ill' I j!JJ d htll d isappeared donicus, R. waterstoni, Larynyssus orbicularis, L. substerna, Sternostoma gradually appmxitn:tlt•ly o1w kilometre boydi. Two duck species (Aythya marila, further out. The· tmhid st�a,water de­ Clangula hyemalis) gave two new spe­ creased the fora , i ng slltTess of the p cies of rhinonyssids: R. marilae sp.n. ducklings but a more serious effect was and R. clangulae sp.n. that the mud-layer cowred the benthic Conclusion: The preliminary analysis of fauna normally calen hy the ducklings. the rhynonyssid fauna of some marine As a consequence tlw ducklings were and coastal birds shows that several emaciated and were apparently less species of rhynonyssid mites are highly resistant to various i nfection s, specific whereas others have a wide spectrum of hosts. In this second group of mites new species can be defined by future studies. 130

CONCLUDING REMARKS

Kurt Buchmann Department of Veterinary Microbiology, Royal Veterinary and Agricultural University, Frederiksberg C. Denmark

During the conference a number of which however are difficult to imple­ presentations have clearly indicated the ment satisfactorily due to the behaviour importance of parasites for the ecology of wild birds. Some extrapolations from and general biology of birds, both from results with domesticated hosts could be terrestrial, marine and coastal habitats. A used to complement the estimation. detailed analysis of parasite communities Another path to use is application of uni­ in birds has revealed the many appli­ que systems. Through the study of wild cations parasitology has in biogeo­ birds with a special biology in nesting graphical, ecological and historical ( crossbills, cuckoo, swifts) information studies. The economic and ecological about susceptibility, vectors and trans­ roles of these birds evidently are of mission of parasites can be achieved. major importance. In this context reinforced ethologial A main question is however posed: studies combined with parasitological How do we communicate all these data (night/day feeding, parasite acqui­ information to other ecologists and sition etc.) will prove valuable. biologists dealing with birds? The advent of modelling of the bird The assembly of parasitologist pro­ ecosystems is highly welcome. However, posed a number of future strategies in due to the lack of studies on mortality this context. A way is to bring ornitholo­ rates these are still less developed com­ gists and parasitologists together in joint pared to human and veterinary epidemi­ projects. These could be based on posing ology. Therefore studies of mortality concrete question whereafter specialists rates should be implemented and erec­ in various fields (including parasitolo­ tion of data bases and cooperation with gists) should be selected for the analysis. computer specialists could improve our The presentation of parasitological knowledge significantly. results should also be presented for the A major future problem was pointed other groups of biologists in a more out. Due to financial problems and visible way. One method could be the budget managements a number of im­ organization of additional meeting of the portant specialists are becoming in­ present type where researchers from creasingly rare. Thus will the lack of various fields are brought together. taxonomists influence the quality of The next important question was then future studies. Likewise, important to outline the future research projects, questions in parasitology, behavioural current problems and solutions. sciences, physiology etc. are often Although reliable indications of solved better through basic studies parasites' impact on birds were presented without unidirectional focusing on short at the meeting we still lack hard evi­ term results. dence on this issue. As a number of The overall conclusion was thus to parameters are likely to influence asso­ reinforce cooperation with scientists ciations found in field studies alternative from a number of other fields in order to strategies should be used. One way is to solve these problems. conduct controlled laboratory studies, Bull s, 1 '1 I \I I i l

TIU< J¥,\ r\ n�· FA t INA ()F COMMON CARP(CY PRINUS CA UrUn I1 1U t A POND IN SOUTH-EASTERN NORWAY

1 2 1 i\pplt'hy and E. Sterud

I! HI v l �ih ' ' ;tiPI y, 1'. 0. Box 8156 Dep., N-0033 Oslo, Norway, itwl y Ml'dicine, 1'. 0. Box 8146 Dep., N-0033 Oslo, Norway

AhNintd l•dlt'\' 1! ti>lll!lll'l! li!! p (('\'fll'iiiiiS However, the parasite fauna of most 1'11/fil!l) I!Pill 1\ '.twdl p!!!!d Ill .'i llltlh· Norwegian freshwater fish species is t·.a.';ln n f\J,Hwd 'H' ,.,,dllllJWd for poorly known (Appleby & Sterud, para:; ill·:.. Tl11n pn1 il'dll '·lll'r'H'S wne 1996). Parasites of wild carp in Norway found: ft·htll\·n/,u,f, , n' , r�ll't . I !t�!'fylo­ have not previously been reported, but gyrus 1//ll'!lo!Uitt.\ illllf r\ t glif!H fo/illi'l'liS. studies from other parts of the world (e. The nJotHlgnwall /.1 11tt1 h1't•lflls was the g. the former USSR) show that the carp most coJll Jnon, and flw nnl lu 1:;t s pecific has a rich parasite fauna (e. g. Bykhov­ parasite. skaya-Pavlovskaya et al., 1962). Introduction The aim of this study was to investigate the parasite fauna of carp The conllno n carp ( '\•fiJ il111s l'lll'fJiO L. from a pond in south-eastern Norway was introdun�d In Ntli WiiV 111 the 1500's which has a dense population of scaled (Peth on, I

Successful nalmal n' Jll oducl ion of carp Materials and methods in Norway h a s on·tiJTed sporadically The study site is a small, eutrophic (Kalas & Johansen, I 9'J5). Lately it has pond on a farm in the municipality of been focused on the possibilities of Racte in 0stfold county, south-eastern exotic parasites being introduced to Norway. The pond is connected to the Norwegian freshwaters with imported sea by a small brook, and is also ornamental fish (Levsen, 1995). In Great inhabited by eels (Anguilla anguilla L.) Britain, introductions of carp have led to and perch (Perca fluviatilis L.) (R the establishment of several potentially Johansen, pers, comm.). The pond pathogenic parasites (Kennedy, 1994), In received fish from Aneboda, Sweden in this respect, a thorough knowledge of the 1956 (Kalas & Johansen, 1995). parasite species of freshwater fish Fifteen carp ranging in size from 128 endemic in Norway is important. to 390 mm and 30 to 839 g were caught 132 with rod and line in August 1996, and Jchthyobodo necator and A. fo liaceus transported alive to the laboratory in could also have been introduced at the pond water where they were examined original stocking of carp. However, as two days later. The fish were killed by a these parasites are endemic in Norway, blow to the head, and all external and and infect a large range of hosts, the carp internal organs were examined for could have been infected by the other parasites under a dissecting, and a phase­ fish species present in the pond. contrast microscope. Bykhovskaya­ Pavlovskaya et al., (1962) was used as a An explanation for the low number of reference for species determinati parasite species found on carp in the Resultsand discussion pond might be that the original stocking only consisted of a few adult carp, and, Three parasite species were found: a due to chance, parasite species may have bodonid flagellate fitting the description been lost if the prevalence in the ances­ of Jchthyobodo necator (Henneguy, tral host population was low. Other 1883), was found on the skin and gills of parasite species may have been present 3 carp (20 %) at low intensities. Seven at the original stocking but may have fish ( 46.6 %) harboured the crustacean failed to establish due to environmental Argulus Jo liaceus (L.) on the gills, oral factors or lack of suitable intermediate cavity and external surfaces; the highest or definite hosts. number found on a single fish was 4. The monogenean ancho­ Acknowledgements ratus (Duj ardin, 1845) was found on the We thank the owners of the farm gill filaments of 13 fish (86.6 % ), the Nedre Stomner for letting us fish in their most infected fish harbouring about 30 pond. Rune Fj ellvang, Rune Johansen parasites. and Trygve Poppe kindly helped with the Dactylogyrus anchoratus is a host­ field work, and Tor Atle Mo commented specific parasite of both common and on the manuscript. crucian carp, Carassius carassius (L.), References and is previously reported from the latter Appleby C, Sterud S. Parasites of white species in Norway (Borgstrom, 1970). bream (Blicca bjaerkna), burbot (Lata lata) This monogenean most probably was and ruffe (Gymnacephalus cernua) from the introduced to the pond at the original river Glomma, south-east Norway. Bull stocking in 1956, since carp from the Scand Soc Parasitol 1996; 6: 18-24 present site have not been in contact with Borgstrom R, Hj elset S, Ravndal J. Karpe crucian carp. Other localities receiving reproduserer i Norge. Fauna 1990; 43: 2-6 carp from the pond in Rade may also Borgstrom R. Tre monogene ikter fra have been infected by D. anchoratus. ferskvannsfisk. Fauna 1970; 23: 183-85 Even if this parasite apparently is not Bykhovskaya-Pavlovskaya lE, Gusev A V, pathogenic (Bykhovskaya-Pavlovskaya Dubinina MN, et al. Key to parasites of et al., 1962), the present study still illu­ freshwater fish of the U.S.S.R. Akad Nauk SSSR. Zoo! Inst, No. 80, Leningrad, 1962. strates the potential danger connected (Translated from Russian by the Israel Progr with the introduction of foreign fish Scien Transl, Jerusalem, 1964) species. 133

Kcttil•'d • d lllltlldllt lltlllS. l n I 't L, r·d·. l';!l :1si1 ic di•.t'il,t ' 1\ddJ•,I!ili!' I .Id I'J'J·l

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PARASITES OF COMMON ASP (ASP/US ASP/US), BREAM (ABRAMIS BRAMA) AND ZANDER (STIZOSTEDION LUCIOPERCA ) FROM THE RIVER NITELV A, SOUTH-EASTERN NORWAY

E. Sterud1 and C. Appleb/ 1 Norwegian College of Veterinary Medicine, P. 0. Box 8146 Dep., N-0033 Oslo, Norway, 2 Central Veterinary Laboratory, P. 0. Box 8156 Dep., N-0033 Oslo, Norway,

Abstract

Asp (Aspius aspius), bream (Abramis prompted the present study of both brama) and zander (Stizostedion protozoan and metazoan parasites of lucioperca) from the river Nitelva in these species. south-eastern Norway were examined for Results and discussion parasites. A total of 33 parasite species were found, 12 of which are new records The results are presented in Table for Norway. and discussed below. Materials and methods Asp, Aspius aspius. The asp Aspius aspius (L.) is one of The monogenean Paradiplozoon the rarest Norwegian cyprinids, being pavlovskii (Bykhovskii & Nagibina, restricted to the south-eastern parts of 1959) is according to Bykhovskaya­ the river Glomma water system. Its Pavlovskaya et al. ( 1962), specific for parasite fauna has never been studied in asp. Characteristic for the species are the Norway. The bream Abramis brama (L.) small anchors and the posterior-most is common throughout south-eastern holdfast clamps being smaller than the Norway, and its helminth fauna has been others. P. pavlovskii and the other studied by Hal vorsen ( 1971) and monogenean found on the asp, Hartvigsen (1995). The zander, Dactylogyrus tuba, are new records for Stizostedion lucioperca (L.), is only Norway. slightly wider distributed than the asp, One adult individual of Phyllodi­ but much more commonly caught. The stomum sp. was found in the urinary zander has been introduced to lakes bladder. P. elongatum Nybelin, 1926 and outside its natural distribution as a part P. fo lium Olfers, 1816 are previously of top-down control projects for reported from asp (Bykhowskaya­ improvement of water quality. No Pavlovskaya et al. (1962). However, the reports are available on its parasite recorded species could not be identified fauna. The poor knowledge of the as any Phyllodistomum species found parasite fauna of asp, bream and zander in cyprinids. 135

Tahlt· oil n'.p L\.lfll/1.1 11.1pius), bream (Abramis brama) and zander (,\'rl. J i! Pill llw liv(�f Nitelva.

•· Nil. , "' w, �<�llf'.<' AI>IHevalions: l•.darvac, m=metacercariae, B=blood, F=fins, !=intestine, K hid!!· , i!\ . \ '>kill, Ill' l!ody cavily, GA=gill arches, GB=gall bladder, GF=gill filaments, I ll I" ·"' f!l,H v ldnddn

llo•.i !lspius aspius Abrmnis brama Stizostedion lucioperca

-� (6) (6) (5) (lllll!ll�t-!\ �Ill!m·dl 459- 1252 532-1336 w. '�'"' 11 dil(.'• ' g g 561-2791 g 390-540 360-460 410-670 I ,, l mm mm mm

""'"'·11· ···'J't ! l! ,, No. i int. site No. i int. site No. i int. site 3 fr \'/ llifit'f l/fi\ fll!/ .,,, + B,K I l't \'f 't!flll\ nfll!! ·,p + B I i\jll!!\tli/Ji! \jl + s 1876 I /, hilil'of'hlhl' 111.1 11111/lifi/iis Fouquct, + GF I

( ;,., '"'"' 1\'lus ,./,•gilns Nordmann, IX\2 I <10 GA 4 I ;,.,,"In• ll'ill.,. '· i'· F Ollcrr/og\'111.1' oun,·u/orus (Nordnwnn, I H:12) 4 <200 GF Oouv/ogyms ru/Jil Linslow, I WJH I < l OO GF /)w:rylogyms 1\'llndni llykhovskii, I 1).\I 4 <200 GF Dactylogyms mndti llykhovskii, I 9.\ I I <5 GF Ancyrocephalus pamdoxus Crcplin, I Xl'l 2 3-5 GF Dip lozoon paradoxum Nordnwnn, I H:L� 2 2 GF Paradiplozoon pavlovskii (Byk. 81 Nag., 3 10-20 GF 2 1959)

Caryophyllaeidesfennica (Schm:idn, I '102) I 2 I Cm)'ophyl/aeus lariceps (!'alias, I 'IX I) 2 1-2 I

Phyllodistollllllll sp. I I UB Phyllodi.I'IOI/111111 1111/lTo<·orrl<' (!)ilw, 1'10'1) I I UB Dip/os/oll/11111 sp. (Ill) 5 5-25 L 2 5 L 4 1-4 L (111) 1 3 Rhipidomlyle sp. + F + F Rhipidocoryle sp. 3 1-2 I 2 2 lchlhyomlylums \'uri<•go/us ( ( 'replin, I X25)(m) + HT + BC,SB,HT 2 2 lchrhyocot\'lums t'iut\'!'1'/'""'us (< 'repl in, + HT + HT 1825)(111) H'itt) I 12 I !11/ocreadium isol"'mln (I -<>oss, I

Phi/omelm ovt/lil (Zcder, I HO.l) 2 1-2 BC Philomelra korlani (Moln:ir, I%')) 2 1-2 BC Camal/anus lili:usrris (Zoega, 177(1 ) 3 1-2 I Camallanus lrul/ca/us (Rudolphi, I X 14) 3 1-2 I I <10 LI I LI Raphidascaris acu.1· (llloch, I 77')) (I) BC, +

Neoechinorhynchus mrili ( Miillcr, I 780) 2 1-4 I

!\eh/heres percarum Nordmann, 1832 4 5-12 OC,GA,GF

Number of species 11 20 9

1 + = Intensity not calculated

2 Full reference to authors in discussion 136

Unidentified metacercariae of Rhi­ the leech vector; experiments not within pidocotyle sp. were found in the caudal the reach of the present study. fin of one individual. We are not aware Trypanosoma abramidis Laveran & of any previous reports of Rhipidocotyle Mesnil, 1904 has been described from metacercariae from asp. european bream, but according to Lom Three female individuals of Philo­ & Dykova ( 1992) this species has to be metra sp. were found in the body cavity redescribed to determine if it differs of the asp. Two species of this genus are from Trypanosoma carassii (Lom, previously known from asp; the host Paulin & Nohynkova, 1980), a species specific Philometra kotlani, and commonly found in different cyprinid Philometra ovata (wide host-range of fishes. cyprinids). Moravec (1994) stressed that In the blood and kidney of bream, we Philometra ovata do not mature in asp; also found a species of Trypanoplasma. only juvenile females are reported. Two One bream harboured both Trypanosoma of the individuals here recorded had and Trypanoplasma. Trypanoplasma partially developed larvae in the uterus. abramidis Brumpt, 1906 has been We therefore assign the name described from bream, but accepting the Philometra kotlani to the species statements of Lom & Dykova ( 1992) that encountered, a species which IS the validity of species descriptions based previously not recorded in Norway. upon host specificity should be The other five species recorded in the questioned, we believe that the species present study have previously been encountered is Trypanoplasma borreli reported from other cyprinids in Laveran & Mesnil, 1902. This species is Norway: Caryophyllaeides fe nnica common in Eurasian cyprinids. The (Borgstrpm & Halvorsen, 1968), trypanoplasm found in white bream, Caryophyllaeus laticeps and Neo­ Blicca bj oerkna (L.), from the river echinorhynchus rutili (Halvorsen, 1971), Glomma was possibly also this species Rhapidascaris acus and Diplostomum (see Appleby & Sterud, 1996). sp. (Vik, 1961). These parasites are also The myxosporean recorded on the known from asp from other parts of the gills is not identified. Some of the spores world (Bykhovskaya-Pavlovskaya et al., looked similar to the spores of 1962). Myxobolus muelleri Biitschli, 1882, which were found on the gills of burbot Bream, Abramis brama. Lata lata (L.) and probably also white Trypanosomes are previously not bream in the river Glomma (see Appleby reported from Norwegian cyprinids. & Sterud, 1996). However, some spores However Appleby & Sterud (1996) in the same plasmodia possessed caudal found a trypanosome, probably projections similar to spores of Trypanosoma acerinae Brumpt, 1906, in Henneguya species. ruffe Gymnocephalus cernuae (L.) in the Six monogenean species were found river Glomma. The present species is on the gills and fins of bream. Diplozoon probably T. carassii. However, paradoxum has been previously reported according to Lom & Dykova ( 1992), from Norwegian bream (see Halvorsen, correct species identification requires 1971; Hartvigsen, 1995), but to the best experimental cross infection studies and of our knowledge, this is the first report also observations on the stages found in of Dactylogyrus auriculatus, D. wun- 137

del'!. f'\ f,,,/,f, t\'111,\ 11ot pnfnrmcd, we report the record as

e!l·gutt lfh !Ill ·.pn it'\ Nhiflidocotyle sp. lt tllll ol' />11, 1\ !ill)'ll! ,ht d Two diffe rent types of digenean /'.:11),1; , H I "jllil;lf(lj I !I metacercariae were found in the present t:till '· llw IVjll' st udy . They could be separated by both spt·• VIII.\' H r• w t·, I /1'1 od,l!l l heir total sizes and the relative sizes of Ntndll!illtn l•w.,•d ttptlll llw �'> their tribocytic organs, and were tvd,··,, 1 HI "I lnllttlwiJ' ( I'J /()) In identified as lchthyocotylurus addtiiPii ' ltllltl !lw 1•.i ll " 111 1 p!atycephalus and I. variegatus (see ;I!I'l l\". dtl tl!ll!l.nlilif'd f ;\'t utfil, 1\'flls sp. Odening, 1979). Metacercariae of I. lwl,lll)'IIW 1" Ill·· Ll�""'llllH nllv dillicull platycephalus have not been reported l ll lll d 1 ,'. I 1 d ,!,'i 11' t i t' I "i I p l P 11 I ltC from Norway before. However, Bakke fill', lltllllL) I. , r\ Ldt!ilt, I (jW\'. < has ( 1979) reported adult /. platycephalus ltlltlld ;1 ·. ttlllliu ··!'''' 11 11il h�t·;llll from from seagulls in south-western Norway. ( ;,.ll ll:tllV nnd •; lt·u Two Camallanus species were found /'h \•f/,,,/, 1/, ,1111111/ lltll• ,,,, ,,rr/1· was in the intestine. Camallanus lacustris is fo11nd 111 tlw lll llli!t V hlndd,·t . This known from a range of host species in species wa!; al:;o tcpt •t kd lwlll white Norway, but C. truncatus, easily bream by /\pplvhy ,\',: �;kl ttd I jll!J(J), and recognized by the truncated tridents of the Phyllot!isltl!ll/1111 sp. '''POI II·d from the head, has previously never been (11)'1'1 ) bream by llartvigs,:n ,., pi()hably reported from Norway. the same spec i es . Of the 33 parasite species found in Zander, Stizostcdion lill'inJ't'lttl the present study, more than one third Only one prolo/.oo:m :.pecks was (twelve) are new records for Norway; found: a trichodinid 1111 tlw ::.kin and gill eight of these are monogeneans. filaments was id<'llttl �t·d a:; l'richodina Although the knowledge of mono­ nigra . 1\ ccord in)', tu l.Pill ,\i Dykova geneans has increased significantly ( 1992) this is a Vt'l y Ulllllllllll species during the last years, this study shows from a whole ran1.'.e 'll I m� I spec ies, but that much is still to learn about the is has pre v iou s l y not IHTil reported from species diversity of this group in Norway. Norway. The same is true for protozoans. More emphasis should be On the i l ti lanwtJis we found the g l put on these groups in future studies. monogcnean 1\nc)•mt't'Jilw/us paradoxus. This is the first record of this species from Norway. Acknowledgements

The trematode Rhipirlocotyle sp. was We thank Eyvind Tomter, Trygve T. found in the intestim�. According to Poppe and Tor Atle Mo, for help with Gibson et al. (I() 92), N. campanula the field work. The latter two also (Dujardin, 1845) is parasitic in zander helped to identify some of the parasites. and perch, while R. fi'nnica Gibson, References Taskinen & Valtonen, 1992 is parasitic in pike. The present species best fits the Appleby C, Sterud E. Parasites of white description of R. fe nnica. However, as a bream (Blicca bjoerkna), Burbot (Lota lata) (Gymnocephalus cernua) total principal component analysis and ruffe from the River Glomma, south-eastern Norway. Bull according to Gibson et al. ( 1992) was Scand Soc Parasitol 1996; 6: 18-24 138

Bakke TA. Iktene Cotylurus platycephalus og C. variegatus funnet i Norge. Fauna 1979; 32: 23-6 Borgstr0m R, Halvorsen 0. Studies of the Helminth Fauna of Norway: XI. Caryo­ phyllaeides fe nnica (Schneider) (Cestoda: Caryophyllidea) in Lake Bogstad. Nytt Mag Zoo! 1968; 16: 20-3 Bykhovskaya-Pavlovskaya IE, Gusev AV, Dubinina MN, et al. Key to parasites of freshwater fi sh of the U.S.S.R .. Acad Nauk SSSR. Zoo! Inst, No. 80, Leningrad, 1962. (Translated from Russian by the Israel Progr Scien Transl, Jerusalem, 1964) Gibson DI, Taskinen J, Valtonen ET. Studies on bucephalid digeneans parasitlZlng molluscs and fishes in Finland. II. The description of Rhipidocotyle fe nnica n. sp. and its discrimination by principal compo­ nent analysis. Syst Parasitol 1992; 23: 67-79

Halvorsen 0. Studies on the helminth fauna of Norway XVIII: On the composition of the parasite fauna of coarse fish in the River Glomma, south-eastern Norway. Norw J Zoo! 1971; 19: 181-92 Hartvigsen R. Spatial patterns In the occurence of freshwater fish parasites. Dr. Scient thesis, University of Oslo, 1995 Lom J, Dykova I. Protozoan parasites of fishes. Amsterdam: Elsevier, 1992 Malmberg G. The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, ). Ark Zoo], Ser 2 1970; 23: 1-235 Moravec F. Parasitic nematodes of freshwater fishes of Europe. Dordrecht: Kluwer Acade­ mic Publishers, 1994 Odening K. A propos de la validite d'Ich­ thyocotylurus variegatus (Creplin, 1825) et de la position specifique de la Te tracotyle ovata (Listow, 1877) (Trematoda: Strigei­ dae). Ann Parasit Hum Comp 1979; 54: 171- 83 Vik R. Parasitter og sykdommer hos vare ferskvannsfisk. In: Jakt og Fiske i Norge, Fiske. Per Hohle (red). Norsk arkivforskning, Bedriftshistorisk institutt og forlag A/S, Oslo 1961 139

soc '11''1 \ ."'l�.··

Fin11l, n .\ !'ill St'fJilmtdy to all members, but we remind

VOII ••!

XVIII u! flw ."·; nuullnavian Society for Parasitology f{fJIHII' Um ulwlm U�·1mmd\ !VIa)· I

Tlw l'l'1/ '>VIIl[" ''"l!ll! •d !lw •;, andlnavian Society for Parasitology will take place in lknllli! lk lh• lwr�Hi ilnl hi.md ol Bornholm placed in the center of the Baltic Sea has lwen l'ho:,nl w.

SL�rvinv. a•; a llitllHr!l lwh I!• .. thn parts of the world. These Scandinavian meetings traditionally lii mv 11 1 lt''•t'iiii'IH'rs in the various fields of parasitology for fruitful discussions ''' all w•P•'; h ,,j p;11asitology. In addition a special mini symposium on human and win tllill ''"Ill• ;d parasitology will be held at the 1997 meeting. Parasitologists will hi! ll w "PJHlllltnity to present new results from their research in various hranvhn: ol tin·. Ill< H'il.'dfi)'.IY important subject, thus providing the latest news about inm11tnity, IIJI >rlndll , dl:t)',nostics, treatment, ecology and other aspects of tropical parasili(' dJsrw,,·;,

General sy111pusilllll IP!JI! will include vaccine development, gene technology, fish parasitology, :11Hllll •I H pm a::itcs, human parasitology, parasitology in wild fauna, a.•;ttol vcteri nary p;u t 'I'S, ho•;t parasite relationships, parasites and the allergic response , inunt11w u·sJHlllst·s to parasites, ectoparasites and vector biology, drug development awl n·sJsl ann�, nutritional aspects of parasite infections and opportunist ic para�:iln; i 11 i mmunocompromised hosts. Specialists in these particular fields have lwtcll invilt•d to give up-to-date reports on the situation in these areas which should attract t·onsidnablc interest worldwide.

Veterinarians, physie ians, biologists, immunologists, ecologists, nutntwnists, physiologists and others will, in May 1997 not only have the opportunity to present their latest findings hut also discuss these with fe llow scientists. At the same time they will become acquainted with a very special island in the Baltic sea.

The island of Bornholm presents its most beautiful sides during the month of May. Flowering orchids and a wide array of song birds will, without doubt, inspire the symposium participants resulting in new contacts, ideas and discoveries. 140

Time and location The 18111 Symposium of the Scandinavian Society for Parasitology will take place on the island of Bornholm from May 22-24, 1997. The Hotel Griffen in R01me has been chosen as an excellent venue for the symposium.

How to get there Participants accepting the entire symposium package will be transported from Copenhagen to Bornholm in a modern ferry equipped with comfortable cabins. If you prefer individual travel there is a ferry from Sweden (Y stad) to Bornholm (Ronne) as well as flights from Copenhagen to Ronne. Please contact your travel agency for these latter possibilities.

Symposium Schedule

We will meet at the get together party Wednesday May 21, 1997 at 9 pm on the ferry to Bornholm (Bornholmstrafikken located at K vcesthusbroen near Set. An nee Plads in Copenhagen). We will then leave Copenhagen and sail to Bornholm arriving on Thursday morning. After breakfast and registration at the Hotel Griffen the symposium will begin and continue throughout the day. On Friday morning the island of Bornholm will be presented for all attendants during a tourist bus trip. After lunch the scientific programme will continue followed by the symposium dinner in the evening after which you will have the opportunity to relax and enjoy a splendid Baltic jazz band. Saturday afternoon the scientific programme will end followed by the biannual session of the SSP. After dinner we will all leave Bornholmon the ferry to Copenhagen, arriving Sunday morningat 6.30 am.

Symposium secretariat

For further information please contact the symposium secretariat:

Danish Bilharziasis Laboratory, Jregersborg Alle 1D, DK-2920 Charlottenlund, Denmark. att.: Grete G�tsche or Birgitte Jyding Vennervald Phone: +45-39626168 Fax: +45-39626121 141 N

l'vl t'lllkl d I<� \llhlllll ill'lllS of news, information on forthcoming lllt'Vfi!W ! ,, ' • !I ptthht nflllll in the News section. Letters and points of view

lo I )unh;h Parasitologists:

In IIJ' u, "nH .t · ;�! fl;lfJt:.h ( 't·ntre for Experimental Parasitology received the ft 1illlWIIIj'

('IJ;u h •lit' f\L11 Id• l lH i· l• wn1, 1'1!.1.>., reeeived the Professor C.O. Jensens Memorial i\ w;ud

Andr1 " l'l'llill!l, ' l'h J; \lwknt l! tT i ved His Royal Highness Crown Prince Frederiks Aw:ud

v,u ;�1.l , ,v,·d 1Vl ana11 . I'll I 1, ' the Young Scientists Award (third prize) of the 1\tlfDjH':!Ill• nlt'Liflll!! f.,, l'a! ;J',ll

Lee Willill)'.h<� lll, l'h 11 •.tttdn!l, n·cci vcd the "Outstanding Graduate Student Award" from the AIIH'IH'Iill v.·tn lii!HV f'vkd ical Association.

NEWS Bait k St·,·t ion

In Mcmodam

Pn>fessor.Jiiri Parn· 1 lh.l uly 1996

.J liri Pane was !Jilt ll •Ht d l:tttn in Yiljandi County of the Estonian Republic (USSR) on 111 October 1 0 , l'l.'X I'J', \he graduated from the Faculty of Veterinary Medicine of the Estonian AI'J ivldtmal 1\ vadcmy with honours. In 1954 he joined the post-graduate course at the I kp:lllllll'llt of Parasitology of the Moscow Academy of Veterinary Sciences, wlw n·. lw IJJ:Itk J\�search on echinococcosis under the supervision of professor 1< ..1 . Skrj:�hin.

Since 1957 lw has lwt'lt working at the Estonian Agricultural Academy and later at the

Estonian Agricultural I J ni versity, first as an assistant, then as senior lecturer, a� sociate professor and professor. In 1958 he received his Doctor of Philosophy Degree and in I l)l)2 h i s Doctor of Science degree. Juri Parre read courses in parasitology (main subject), veterinary genetics, poultry diseases and fish diseases. He has published about 250 papers and articles and also parasitology textbooks. Over many years his main field in research was chicken eimeriosis, where he made excellent contributions. I le was the chief editor of the Estonian Veterinary Review 1989-1995. Since 198<) he played a major role in establishing collaboration with the Scandinavian countries, especially with Denmark. 142

FAO-support to research and control of helminth infections in Lithuania Consultanship from and collaboration with Danish Centre for Experimental Parasitology Following independence, the agricultural sector of Lithuania underwent dramatic changes from large scale collective farms to privately owned mostly small holdings with diversified crop-livestock production. Consequences of these changes are many and varied. With the change of management most of the ruminants are now kept on pasture during the summer and confined during winter. The result of this is a clear increase in pasture related diseases such as gastro-intestinal nematode infections. Currently, the veterinarians are not able to advice the farmers on how to efficiently control parasites in their herds and flocks. One of the reasons for this is the lack of basic epidemiological knowledge. There is an urgent need to address the training of the private and state veterinarians in new, appropriate technologies and disease control strategies. The objective of the project is to improve livestock production by establishing epidemiological and production data by monitoring the natural occurrence of specific parasitic infections, and in collaboration with private and state veterinarians to evaluate the effect of different control strategies. To achieve this, a FAO project (Technical Cooperation Programme) will provide the services of consultants, and funds will be made available for the purchase of supplies and materials and laboratory equipment. The project will also cover the cost of in­ service training courses and training abroad, as we11 as official travel, administrative assistance, and general and direct operating expenses. Danish Centre for Experimental Parasitology, acting as a FAO Collaborating Centre in Helminthology, will provide consultanship and training, and will assist in planning and implementation of the project, which receives a FAO contribution of US$ 177,000. Dr. J.W. Hansen, FAO 143

t t U Ll ES FOR CONTRIBUTORS

I ·c�dn,,Jtlnl a.o.; word-processed manuscripts on floppy disk, !il l llllll I lll·l!t IHili' print outs of good reading-quality. The prefen·ed

,•;! lll !1 di· I 111 fV1 S ·DOS or MS-DOS compatible format. The text :,iltH!Id I 111 W Prd Pcrlcct or other word processing programs ('1>11\'!'l!d !\ladnlosh computer, save the file in the MS-DOS t'!Hill!i!llhh tillll! .11!" till' word processor (and version) used to generate tlw Id, "!Hl•\lkl !lw lljH.' Jaling system, and the formatted capacity of the di·J••II,

llw •H IP J, "llllWHII! ni !I HI'• :. hu11ld normally not exceed 4 printed pages, including tahlt· ., I 11' '11' nud 11'1! H I!! .nul may contain a maximum of 2000 words if there are I h 11u IV! lP "' t•dil• Ill' lw.t png1· :; ould show the title of the article, and the name(s) ut tlw t�uthul! 1 lit• ,� u!lun•,' addH'Sst:s should be given, and the complete correspon­ d<'ll• l' ;HI.h. n:tll!I• kl'hntw ;uul l<·ldax number (if available). The text should follow, '* ·,hi ll a wllltulli '.tt!.l!. "' h111 I S ll l nll J ry, rnaximum 100 words, may be included.

Tlu· I• ·hnuld I unp1stiliL�d (unaligned right margins), without hyphenation ;md at I (<'>�<1. ·pt ' "' ' "'lli'"lll!d nd., ), 1/z line spacing. Do not type page numbers. Label tlw h;11d • ll!Jil , I hand nl llw IH>II um of the page. Please ensure that the digit 1 and the ktli·1 'I' hil'' I n u·,.·d ptl!jlt'iiY,li kewise with the digit 0 and the letter '0'. Do not use Hill ld e de,·, I l"! lllill! !!II' . "''' 11 w• h() fac and centred headings, or underlining of titles or Slthhc;uh

Attlh()lc. IPllmvth e ""' l)hlw�·d 11) ru les governing biological nomenclatures, as laid down in 1' I' llw lllfnnufluwd ('or/(' (!f' 'LoologicalNo menclature. Disease names should folluw tlw pl llll tpl,,, 1 d StiJIIdun/i;:erl No menclature of Parasitic Diseases (SNOPAD).

Fir.11n: lt.'I'YIHb tnw.t lw inc l uded on the diskette, but the figures will be handled conv{·nlioually. Tlwy :;luHIId lw 111arkcd on the back with the title of the article and name of tlw (lust) authPt

Line drawings �.huttld ht· provided as good quality hard copies suitable for reproduction as suhtnillcd.

Photographs must ht· provided as glossy prints, and be of sufficiently high quality to allow reproduction on standard (not glossy) paper. Colour plates will not be printed.

References in the ll'xt shold be stated by giving in brackets the name of the author and the year of publication, e.g. (Thornhill, 1987) or (Austin & Austin, 1987). If there are more than two authors, only the first name plus et al. is given (Lund-Larsen et al, 1977). The reference list should be in alphabetical order, and follow the style set forth in Uniform Requirements to Manuscripts Submitted to Biomedical Journals, Br Med J 1988; 296: 401-5. References to journals should contain names and initials of the authors, article title, the abbreviated name of the journal, year of publication, volume, and first and last page numbers of the paper. Journals should be abbreviated according 144 to the "List of journals indexed in Index Medicus". Authors without access to this list may type the full name of the journal, and the Editor will take care of the abbreviations. If there are more than six authors, list only the first three and add 'et al'. Personal communications and unpublished data should not be used as references, but may be inse1ted in the text (within parenthesis marks). Examples of correct forms of references are given below:

Standard journal article: Anonymous. Some facts on small animal practice. Vet Rec 1987; 120: 73 Horsberg TE, Berge GN, Hoy T et al. Diklorvos som avlusningsmiddel for fisk: klinisk utprpving og toksisitetstesting. Nor Vet Tidsskr 1987; 99: 611-15 Lund-Larsen TR, Sundby A, Kruse V, Velle W. Relation between growth rate, serum somatomedin and plasma testosterone in young bulls. J Anim Sci 1977; 44: 189-94

Books and other monographs: Austin B, Austin DA. Bacterial fish pathogens: disease in farmed and wild fish. Chichester: Ellis Horwood, 1987 McFenan JB, McNulty MS, eds. Acute virus infections of poultry: a seminar in the CEC programme, Brussels 1985. Dordrecht: Martinus Nijhoff, 1986. (Current topics in veterinary medicine and animal science 37) Sosialdepartementet. Tsjernobyl-ulykken: Rapport fra Helsedirektoratets didgivende faggruppe. Oslo: Universitetsforlaget, 1987 (Norges offentlige utredninger NOU 1987: 1) Thornhill JA. Renal endocrinology. In: Drazner PH, ed. Small animal endocrinology. New York: Churchill Livingstone, 1987: 315-39

The manuscript (diskette and paper copies) should be sent to the editor in your country, see inside of front cover. Label the diskette with the name of the (first) author. Manuscripts are accepted for publication after review and recommendation by the Editorial Board. Authors will be notified by the Editor-in-Chief about final acceptance and expected time of publication.

REPRINTS WILL NOT BE A VAILABLE.

In the interest of speed, no proofs will be sent to authors. It is therefore of vital importance that the manuscripts are carefully checked before submission. BULLETI N ( }f' i m l<:dlior

Ill'.! IHJ

Demnm h: I l!lll•ki ',I'IL Fl enmHnv I ' , l>t-pl of. Vet. and 010/ ( >slo for /,tJ!!I In"' "ll'li fiJ, '' I I' Mokt !111 lJ ' 1 13, IlK I (Tcl: l ,, ., +45 \') e�r11ail H

Ja�gc1 :;hql DK·)VJn ! IHH (Tcl: l ,J +4.5:\'l(l ,l (! l l! biladhlpi,;•t"'l'

Eskild l't'li p,, n Scrumin·d Hill, I Parasitohlb' V. I Copcnhar<' ll ;, (Tcl: l'l'l \

+4.5 UilH \!) \ I I !wl!n

Finland: d " ' I T. hcl ics,

Margatt'llii! ! lt� .l ;d 11w llc',nllch, Abo J\kndctnl l' ·I ,, \ /I

Bioi., Ill! H '! I I ; d ( I.\ I 11I ')}1 1 >) I KO, \'\ 6, FIN }w, .•n i I j \')/ /) t' flli!il:

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212(J511 /iJ l !' IILH I magustal iilf tohillll I, 11!int ut Uallk Nnv,�: n. l lnll!:.h ( 'tt of Hannu Kylim''''l'l'li d, li uvnl Vt·l

Sairaal n , Nwdcit''� 1< I !,nv l!tilow:;vej 20, llh f!l !'1 ,·.jf!�. ;;I H'IV FIN-00)')0ll r.+.;�nl, ! I

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+358 () •11 ()) '1 ) l BULLETIN OF THE SCANDINA VIAN SOCIETY FOR PARASITOLOGY

VOL. 6No. 2 CONTENTS November 1996

Proceedings from SSP special symposium: Parasites and ecology of marine and coastal birds, Stykkish6lmur, Iceland 15-18 june 1996

Karl Skfrnissonand ArneSkor ping (Editors) ...... 1

The parasite fauna of common carp (Cyprinus carpio) from a pond in South-Eastern Norway.

Chris Appleby and Erik Sterud ...... 131

Parasites of common asp (A sp ius aspius), bream (Abramis brama) and zander (Stizostedion lucioperca) from the river Nitelva,

Erik Sterud and Chris Appleby ...... 134

NEWS

XVIII Symposium of the Scandinavian Society for Parasitology,

Bornholm - Denmark, May 22-24, 1997 ...... 139

Prestigious awards to Danish Parasitologists ...... 141

Baltic section

In memoriam, Professor JiiriParre ...... 141

FAO-support to research and control of helminth infections in Lithuania ...... 142

Guidelines for contributors ...... 143