THE METAZOAN PARASITE FAUNA OF GREBES (AVES: PODICIPEDIFORMES) AND ITS RELATIONSHIP TO THE BIRDS' BIOLOGY
BY ROBERT W. STORER
MISCELLANEOUS PUBLICATIONS MUSEUM OF ZOOLOGY, UNIVERSITY OF MICHIGAN, NO. 188
Ann Arbor, May 31,2000 MISCEI.I,ANEOUS PUH1.IC:ATIONS M'IJSEIJM OF %OOI.OC:Y. LJNIVERSITY OF MICIHI<;AN NO. 189
Tlic pl~blicatiorisof' the Museuni of' Zooloky, The IJnivel-sity of Michigan, consist primarily of two series-tllc Occasional Papers and thr Miscrllaneo~lsP~~l)lications. Kotli series we]-c founded by 111: Rryir~ltWnlkcl-, Mn Bradshaw H. Swales, and Dr. W. W. Newcomb. Occasionally the Mt~set~nip~~hlishes contribtrtions oc~tsidcof these series; begirir~irigin 1990 these are titled Special Pr~hlicationsand arc numbered. All sublnittcd rria~iuscriptsreceive extel-nal review. 'Tlrc Miscellaneous P~~l)lications,which include monographic siltdies, papers on field arltl I~II- scum tccll~liques,and other contributions not within the scope of the Occasional Paper-s, ar-' pub- lished separately. It is not intended th;lt they 11c grouped into volu~ries.Each riun~bel.has a title page arltl, wlicrl ~iecessal-y,a tal~leof contents. The Occasional Papers, ptlblicatio~iof' wliich was bcgun in 1913, senTeas a niediuni fol- 01-iginal stt~dicsI~ased pl-incipally upon the collectiolls ill thc MIIS~III~I.Tliry al-r isst~rdseparately. Whc~la sr~llicirnttlu~nbt-I- of' pages has been printed to make avolunie, a title page, tahlr of'contents, ;inti an i~~dexitre supplied to libraries arid individuals on tlie mailing list for the SCI-ies. A cornplctc list of publications on Birds, IFislics, Insects, Ma~r~~nals,Mollusks, Rcptilcs ii1lt1A~iipl~ib- iaris, ~u~tlother topics is availilblc. Addl.css inquiries to tlie Director, Musr~~rnof'Zoology, The Univcr- sity of' Michigan, Ann Arhor, Michiga~i48 lo!)-1075).
Bailey, K.M. & (:. G;rns. 1998. 'live new syril~ra~~c.hitllishes, Monop/(~v.rro.sr,li from Pc~lills~~la~.l~ltlia iu~dM. rlurilr~c~ifrorii Sri I;ark;~. Occ. Pap. 726. 18 PI)., 7 figs $2.00. Nr~ssl)a~~rn,R.A. Xc M.E. Pfrctrdcn 1998. Revision of'tlir ASI-ican caeci1i;in genus Schis/o?nrlopclrnParkel- (hriipliibia: <;ymnol~hiori;l:(:ileciliidac). Misc. Pul~l.187. 35 pp., 15 figs., 15 tables, 2 color plates. $7.00. Wc1111, S.A. arltl li.1i. Miller. 1998. %oogonc,~ir~is~~quilc~, a ticw goocleitl Gsli ((:yp~-i~~odor~tifo~-~iies)ft-om the Alncca tlr;lin;~gcof Mcxico, iind ;I rediagnosis ofthe grnrls. Occ. I'ap. 725. 28 pp, 5 tigs. $2.00. Ntrssbatun, R.A., (::I. R;rxworthy & 0.Pronk. 191-18. Tlre ghost geckos of' Madagascar: a fitrtlitu. rcvi- sion of tlie Malagasy Icaf-toctl gcckos (Reptilia, S(l~~;imata,Gekkonidae). Misc. I't1111. 186. 26 pp,, 25 figs., 5 tahlcs. $9.00. Dyrt; R.S. 1997. Pliylogenetic Revisio~iof Atherinopsinae ('kleostci, Athcri~iopsidae),with (;otil- IIICII~S011 tl~cSystcniatics of tlie South American FI-esliwatt-I.Fish C;c~rttslIn~ilicli~bhj~,\ ((;i~.a~-tl. Misc. Publ. 185. (54 pp., 46 figs. $15.00. OCol~rlor;R.M., R.K. Colwell 8c S. Nacem. 1996. 'rlir Flower- Mires ot..Ii-inid;ld 111: 'I'lic Gc~it~sIil~ino,c(,iut (Acari: hscidae) . Misc. 1'11111. 184. 32 pp, 70 figs. $10.00. ILlr~gr,A.G. & K.A. Nt~ssbaurri. 1995. A Review Of APr-ican-Madagasci111Ckkkonid I.i/a~.tlPhylogeny A~idBiogeogl-aphy (Sqlrarnata). Misc. Plt111. 183. 20 pp, 11 ligs. $8.50. Kaxwortlly, (;.J. & R.A. Nussbaum. 1994. A review of. the Madagascan Snake Gcncl-a l's~urloxy?-hoj)z~.r, I'~~m~-l~(~rlin(~m,i11itl IIc~tmliodot~ (Squ;im;~t;t: (:olubr-idae). Misc. I'uhl. 182. 37 pp, 25 figs. $1 1.50. Gosli~~e,W.A. 1993. A sr~rvcyof ~~pprr,jawm~~scr~laturc in 1iiglic1- tclcostca~i fislics. Occ. Pap. 724. 26 pp, 9 figs. $2.20. l~~rrllrn;~n,M1.E. 8c J.A. (:arnpl)ell. 1992. Hylid frogs of tlic ge1111sI'l(~c-lrol~~lrr: Systc~ri;~tics a~ltl phylogc- nctic ~.clationsllips.Misc. 1'11111. 181. 38 1111, 2 1 figs. $9.10.
I.cc (:. Bollitlgc~,(,x o//itio 1);unic.l I). Hal-ning, C:l.;ltl(l H~I\TII At~drca17iscl~e~~ NCWIII~II, AIIIIAI l)os D;~vitlA. B~-;~l~tlon,Ann i\~-ho~- OIi\rii~1'. IVI~I~I~;II-~,(;oo(i~-i( 11 S. MAI-~~II131ylo1; Grossc I'oinrc F;u-lirs 1.;1t11.c11ecB. I)citch, Rloomlicld tlills liehecc;~RI( (;owan, Ann AI-bol- I<,ithc~-i~icI<. White, AIIII R1-1,ol. The Metazoan Parasite Fauna of Grebes (Aves: Podicepediformes) and its Relationship to the Birds' Biology
Robert W. Storer
Bird Division Museum of Zoology The University of Michigan Ann Arbor, Michigan 48 109-1079, USA
MISCELLANEOUS PUBLICATIONS MUSEUM OF Z00L2OC;Y,UNIVERSITY OF MICHIGAN, NO. 188
Ann Arbor, May 31, 2000 Tllc lilk cycle of the ccstodc, ?ic/rin hir~mls. Thc adult parasite (centel-),whicll reaches a length of approximately 2.5 Irlln, irlllabits the anterior section of the small intestine of the definitive host, herc an Ez~redGrcbc (I'odicc~j~st~ipicollis). A mean of 2,794 individual worms of this species has becn Pound in 31 individual birds. The minute (0.02 mm) eggs are passed into the wateI; where they arc presumably swept into thc moutl~ofthe intermediate host, a corixid bug (Sigma), by the insect's front legs. Grcbcs become infected by eating the bugs, which may teen1 in lakes where the birds breed. This common parasite of grebes in the Northern Ncrnisphere belongs to the fi~rnilyAmabiliidac, all br~tone ofwl~osc29 spccies are grebe specialists. Origi~ialdrawing by Jollil Mcgahan from sources listed ill thc acknowledgrnents (p. 65).
ABSTRACT
Slow); li. W 2000. 7'1~~M(llnzoc~17 frarc~.sil~/(~una (~gt-(,he.s (A~J~s: I'odi~ij~rdi/oi-rn(~,s) rind its ,rrlalion,ship lo th~ hir.(islbiology. ~Misc.I'r~bl. Mus. Zool., CJniv. A!lichigc~17,188:l-90, I O,figs., 7 tabl(~s.The data base of this work consists of a list oP thc n~~rlticclll~larparasites known to infect grcbcs and a list of the known spccics oS prey taken by ?ac:h specics of grcbc. Tllc formcr inclltdes information on whcrc in thc bird the parasites arc fo~~nd,the distribution of the parasite species by continents, degree of host specificity, and life cycles (whether on fresh or salt water and lists of known intermediate and paratenic hosts). These data sets are used to sl~owhow the parasite faunas arc related to the biology of the birds. The aquatic existence of grebes and the widc range of prey taken by individ~~alsand spccies of grebes are reflected in tlic wide range of helminths infecting the birds (113 species ofdigencs, 86 ofccstodes, 13 of aca~nthocephalans,and 37 of nematodes, most ofwhich have aquatic lifc cycles). One family, one subFC~rnily(each with the exception ofa singlc spccies), several genera, and 104 spccics of'hclminths are considered grcbc specialists, as at-e most ofthe specics of cctoparasitcs. Of the well-studied species of grcbc hel~ni~itlispecialists, almost all have been found in more than one gl-cbc spccies and Inany rnorc in more tllan orlc grebc genus. This is believed I-elatedto tllc fact that even grebes adapted for taking particular kinds of prey will usually take Inany other kinds. Thrrs, where several species of grcbcs arc sympatric, thcrc is a considerable ovel-lap in diet and consequently, ovcrlap in the intermediate hosts ingested. On thc other hand, most of the ectoparasites appear to be confined to single grebe species. Grebes contain large 11urnbcrsof intestinal lielminths. In a study of these parasites of 91 grcbcs from the breeding grotmds in Alberta (Stock 1985), all were found i~~fectcd,with nr~ml~ersranging from 2 to 15 specics and 112 to 33,169 individuals, the majority (96 percent) of which were cestodes. Most grebes spcrld the breeding season on eutrophic bodies ol'watcl; which have an abundant supply ofkinds and individuals ospotcntial prey for the birds. More than half of the spccies of grebcs winter on salt water where a variety of hcl~nirlthswith salt-water intermediate 1.1ostscan infect the birds, bl~ttlnfor- tl~nately,very Pew grebes taken on salt-watcr habitats have been examined for p;~r;isites. Still other kinds of'helminths may be acquired on bodies of watcr along the birds' migration routes. Most of the helm- i~lthsthat are obtained on fresh waters presumably are lost shortly after the birds' arrival on salt watcr and vi~pII(~T,S(C. What causes these changeovers in unknown, but it is suggested that the n~cchanisrnsfor this are I-eversals of the salt gradient in thc intestines. Eared Grebes coming to the highly salinc Mono Lake 011 their molt migration after the breeding season presumably soon lose their Iielminth parasites. Grebes have a u~~iquchabit of swallowing their own feathers which form pellets containing other indigestible materials and, when cast, arc believed also to rid the stomach of nen~atodcsthat Seed on the grebes' food therc. A separate plug of feathers is lodged in thc pyloric outlet of'the stomach where it acts as a sieve preventing large pieces of iildigestiblc material from passing through the intestine. This is bclicved to reduce the likelihood olpa~.asitesbeing dislodged from the wall of thc gut. Grebcs arc the only birds that do not nest on land but regularly build floating nests of matel-ial taken from the water. As a consequence, they are not known to be parasitizrtl by animals like flies, fleas, bcdbugs, and ticks that require a stay on land as part of their life cycle, and because of their limited physical contact with other birds, bnt few specics of cxtcr~lalarthropod parasitcs (12 mites and 13 lice) have bee11 reported SI-om thcm. I~lfectionsby several of these external parasites are thought to have resulted 11-om crossovers from coots (Pltlica). Although grebcs are found on all continents except Antarctica, with a minirnr~mof three species on each, studies of their parasitcs havc been few outside of the Northern I-Iernisphcl-e. This is especially u~~fortunatebecause the greatest numbers of grebe species and c~ldcmicsare fotnld in South America. Thc virtual lack of infor~nationon the parasitcs of' these birds severely limits the potential for parallel studies on the evolution of grebes and their parasites. Thc parasites of grebes offer many possibilities for research from regional surveys and working out life cycles to stuclies on biogeography and evolution of these animals. A data base for the parasites is available on the web. CONTENTS PAGE
ABSTRACT ...... ii INTRODUCTION ...... 1 M. ijon SouncEs ...... I GI~EI~ES11s Hosrs (11, PAI MI~~II~I)S...... 4 TIIV.SCII. .NTIFIC AND ENGI.ISIINA~IES OF 6111..I~ES ...... 6 THE PARASITIC WORMS Oli HELMINTI-IS OF GREBES ...... 7 TIIEDIGENES (DIGENE~I~ . TI I-Iclmirlrhs ...... 58 External I'arasites ...... 59 Futttrc coevolutionary studies ...... 61 ~I<~s~~.W~\.);:EI FIGURE PAGE The life cycle 01' the cyclophyllitlcall tapeworm. Y'ntria Oir~mis...... Cover Legend Sot- cover illustration ...... ii Tlle lire cycle oS the digenc. l'elnsigor 'nilidus ...... I1 The life cycle of the digclic. Slrig~cc/nLo?zis ...... 15 The life cycle oS the pseudophyllidean tapeworm. Srhisloc'f11~r~L1i.ssolidus ...... 19 The lil'e cycle of the cyclophyllictean tapeworm. Sclzi.stotn~nia t~nuicir,.u.s...... 21 Tlle life cycle of the acantl-~ocephalan.Corjlnosomc~ .slrunzo.s I~VL...... 27 Adaptive radiation in the 1)ill form of grebes ...... 44 An ~~nrootedtree showing the relationships arnong illc gcncra and species of grebes ...... 47 Some species of amabiliid cestodes ...... 71 Three lines oS grebes ...... 57 TABLES PAGE 1 The Uistribu~ionof Grebe Species ...... 3 2 'The Diversity of Helminths in Grebes and Alcids ...... 42 3 Numbers of' Named Species of' Parasites Reported horn Each Grcbc Species ...... 43 4 Nunlbers of Named Species of Parasites in each Majol . Parasite Croup Reported Srom each Grebe Species...... 53 5 Nunibers of Grebe Helminth Species in each I-Iost-Specificity Category by Family ...... 54 (5 Thc Distribution of Mite Species on Grebes ...... 58 7 Distribution and Hosts of' Lice of the (:enus Aqunnirn111.t ...... 59 INTRODUCTION On a broader scale, parasitology is one of the most inte- grative areas of biology. In particulai-, helininth parasites can In preparing accounts of grcbes for the North American "provide a new dimension to understanding ecological in- Bird Biographies (Storer 1992; Storer & N11echtcrlei111992), teractions, patterns of distribution, and the complex history 1 f'o~~rltlno gcnct-a1 lists of grebe parasites. While hosts are of many geographic regions and biotas," and because they regularly listed in studies of parasites, lists of parasites in- are "indicators of the historical and ecological development, fecting an avian host or Fanlily of hosts are rare, and studies temporal longevity, current health, and prospects for conti- on the relationships between the avian hosts' biology with nuity of biotas" they are important in studies of biodiversity thcir parasite Saunas, scarcer still. (I-Ioberg's study of the platy- and in pointing out critical areas and biotas to conservation- hclminth par;lsites of tlle Alcidae [I9841 is a notable exccp- ists (Hoberg 1997). Lion.) The unique or unusual aspects ofthe biology of grebes Most helminth parasites, which constitl~tcby far the larg- that might affect their suitability as hosts for internal or ex- est number of species parasitic in grebes, pass through one or more inter~nediatehosts before reaching the definitive ternal parasites present an unusual opportlrnity to investi- L2 gate how the life style of a group of birds may be related to grebe host. 13ecause the last intermediate host or a paratenic that of' the birds' parasite fa~una. host must be ingested by, or otherwise reach, a definitive The grcbes have no known close relatives and are hosts to host in order for the adult parasitc to develop, it is clear that sevcral groups ol' parasites seldom or never Sound in birds of parallel lists of intermcdiate and paratenic hosts known for otl~crgroups. Altl~o~rghno general assumptions can be rnade each parasite and of the prey species known for each species regarding coevolution of parasites and their hosts (Hoberg of grebe are needed to determine what parasites might be PI (11. 1997), how the evolution of tllesc groups may have pro- expected to inf'ect any grebe species. Conversely, the pres- ceccletl is of considerable interest and may provide clues to ence of a parasite in a grebe may be useful in indicating con- the hosts' rcl;~tionships(Brooks & McLennan 1993; Raer 1957, sumption of a species of iiitcrmediate host that might not for ccstotlcs; Clay 1957, f'or lice). have been found in examination of stomach contents of the Quite asitlc from their evolution in grcbes, the parasites bird. have m11c11 intrinsic interest. For instance, parasitic worms The more deeply I went into parasitology, the more ques- or hellninths, usually have complex life cycles requiring one tions arose about the relationships between the parasites and or more i~ltcrnlccliatehosts bef'ore they can infect the de- their hosts. These in turn led to ideas about what might be Gnitivc host in which scx~lalreproduction takes place. Their done with the information I had been collecting.- What startcd inl'cctivc scagcs may also be accumulated in paratenic or "trans- out as a simple list has led to sets of data which could be port hosts," which differ from intermcdiate hosts in that no analyzed in various ways and which could be expanded as further development of the larval parasite occurs within them. new information became available. I am unaware that a similar Tllcse infective stages are often found in fishes. Because grcbes study has bcen designed for any other group of birds and serve as definitive hosts for parasites of those intermediate suggest that this work, with suitable modifications, might be and paratcnic hosts, they inay adversely affect fisheries. Thus, useful in planning future studies. their parasites liavc bcen much studied in countries with Major sources. Rausch (1983) presents an excellent sum- important fr-esll-water fisheries. mary, including a brief history, of our knowledge of the biol- Uecausc the terins intermediate host and paratenic host ogy ol avian parasites. Yamaguti's Systeino Helminihunz (1958, arc clefincd fi-on1 the point of view of parasitologists, I think 1959, 1961, 1963). contains world lists of the helminths and it advisable to use tlie term infective host for any carrier ofa thcir vertebrate hosts and is basic in summarizing informa- stage that may infect an avian host. These may be the last tion up to the dates of the publication of the various parts, intcrmediatc host or pat-atcnic hosts or both. For those study- and Yamaguti (1971, 1975) updates the trematode volume ing the avian host, it is ~lsuallynot significant which. of this work. The supplements to the Index-catalogue of Thc Inore that is known about the biology of a parasite, Medical and Veterinary Zoology (U. S. Dcpt. Agric. 1966- the more wc can learn fro111 it about the biology of its avian 1984) provide lists of hosts for parasites. BaruS rl (11. (1978) hosts and vi~e~~er,sn. Itlcally, we should know not only the for the nematodes and Ryzhikov el al. (1985) for the cestodes identity of each host in the parasite's life cycle but also the and acanthocephalans also have been indispensable for this behavior ofthe li-ee-swimminglarvae, how the parasitc is trans- study. Dubinina's thorougli monograph of the Ligulidae mitted to each stage in thc cycle, the habitat in which this (1980) contains a wealth of information on this family of occ~n-s,the specificity and range (both ecological and geo- cestodes, and Ryzhikov & Tolkacheva's (1981) revision of the graphic) of each liost. When these data are known for a spe- Acolcata is an up-to-date work on the systematics of the cies or group of birds, a surprising amount of information Amabiliidac and Dioccocestinae, the two groups of cestodes can be obtained froin determining the parasite load in a sample which, in the adult stage, are almost entirely confined to grebes.- of' a single species of definitivc liost. Bartoli's (1989) study Valuable sources of information on life cycles are Schell (1985), ofthe digcncs found in a breeding popnlation of the Yellow- Shoop (1988), andyamaguti (1975) for digenes, Mackiewicz legged Gull (I,anis ccichinnnns michnhellis) in Sardinia showed, (1988) and Schmidt (1986) for cestodes, and Alldcrson (1988, among other things, not only what the birds were eating but 1992) for nematodes. Hylnan (1951a,b) contains valuable in what habitats, dill'erenccs in foraging between the sexes, information on the biology of the helminths up to tlie time and whence some of'the birds came to the breeding grounds. of its publication. Crompton & Nickol (1985) provide an up- The llse of such a broad spcctruln of information is natural to-date account of the biolocgy of acanthocephalans, and Sawyer history in the best sense. (1986) of the leeches. Brooks rt 01. (1985,1989) and Adarnson 2 M~sc.Pus1 . Mus. ZOOL.,UNIV. MICH., NO. 188 (1987) present pllylogenetic analyses ofthe rnajor gronps of among these seven genera arc sufficient to place them in tlre digenes, and the nematodes, respectively. I-Ioffrnan (1967) two or three groups or tribes (Storer 19631)). There is thus a is a uscfl~lsorlrcc of information on the spccies of fishes known range of levels of relationships within the family from that to be hosts of helmintll larvae and McDonald (1969) for in- of a tribe to that of subspecies. Grebes are found 011 all formation of parasites of waterfowl also known to parasitize continents except Antarctica, with a minimum of three species grebes. The theses by Galli~nore(1964) and Stock (1985) on each. Several species are found on islands, and three flight- contain n111c11 basic data on the intestinal helminths of North less or nearly flightless species are or were confined to single American grebes. For the lice, the check-list of Hopkills & lakes or lake systems. A list of the species and their distributions Clay (1952),altho~~gh long out of date, is still a major source is found on Table 1. of informatioil on that grol~p.Ash (1960) presents a general Grebes probably arose in South America, where nine spe- account of the biology of licc inhabiting birds. Edwards' re- cies, six of them endemic, are found. These endemics in- vision of ilqunnir.rnu.c (1965), the species of which are only clttde the only two spccies of liollnndicr, which is believed to linown fi-om grebes, is of special interest as the only study of be closest to the ancestral stock of the (Storer 1976; a group of licc which is considered to have speciated on grebes. Fjeldsi 1977) and the monotypic genus 1'odicaf)horus. The mite genera, Rl~i~~o~i,yssusatldPtiloxunus, have also speciated The age of the group indicates that there was ample time on grebes and when better known, rnay well offer opportu- for grebes to acquil-e parasites or for sltbs~antialcoevolution nities for parallel phylogenetic studies with the grebes. Bush to occur between hosts and parasites. Additionally, the wide ut ccl. (1997) give uscf~~ldefinitions of population and conl- geographic distributions of some grebes rnay enhance expo- mnnity tcrnrs often used by parasitologists. sure to infections by a broad variety of parasites. The differ- Grebes as Hosts for Parasites. The grebes form a well-de- ences it1 parasite diversity between widely distributed spe- fined and ancient avian fainily with a world-wide distribw cies of grebes and those endemic to single lakes or islands tion. They were long tllought to be nearest to the loons offer possibilities for comparisons. (Gaviidae), and this view is still held by some (~.g.,Cracraft In size and diversity, the family of tlre grebes, the 1982). On the other hand, molecular evidence supports the Podicipedidae, is comparable to that of the strictly marine view that grebes have no close relations anlong Recent birds diving birds, the Alcidae, the parasitcs of which have been (Hedges Sc Sibley 1994). Altlrol~ghthe known fossil record studied extensively by Noberg (1984, 1986) and with which of the group only goes back to the Oligocelle (Nessov 1992), interesting comparisons might be made. the known fossil grebes are not snfficic~ltlydifferent f'rom Parasite faunas reflect the habits of the hosts. Grebes, which Recent ones to provide clues as to what the grebcs' closest may seldom, if ever, come on land, are ideal hosts for para- relatives might be, and 011 the basis of DNA-DNA hybt-idiza- sitic worms with aquatic intermediate hosts. Grebes feed al- tion studies, it is believed that grebes diverged from a basal most exclusively on aquatic animals, and the eggs of the para- stock of modern birds earlier in the Cenozoic than the sites are excreted by the grebes directly into the water where Oligocene (Siblry & Ahlqnist 1990). they or their larvae can infect intermediate llosts. It is not The morpliology, beh;~vior,pattern of tllc downy young, surprising, therefore, that grebes carry a heavy load of tape- ecology, and food habits of many of the spccies have been worms. It is not unnsual to find large numbers of several studied, and there is general agreement on the phylogcnetic species of this group of parasites in the intestines of a single relationships amoilg the species (cf. Storer 1967a, 1976; Fjeldsi bird (Stock 1985). The diversity of inter~lalparasites is in- 1977, 1985), but to date, there have been no nlolecular studies creased in the grebes that breed in fresh-water habitats and which night be used to test these rclationsl~ips.In addition, winter on salt water, because each of these habitats has its a major limitation for making studies of co-speciation and own contingent of parasites and their intermediate hosts not historical biogeography is the virtual lack of information on found in the other. The long associati011 between these para- the parasite faunas of grebes in South America, which is sites and grebes is reflected in the large proportion of the believed to have been the center of radiation ofthe family genera and species of tllesc worms that specialize in grebes. (see below). Stock (1985) presented s11cIl a study, but it was Grebes' habit of picking up land-based insects from the based in part on Fig. 11.17 in Rich (1983) showing that five surface of the water or from emergent vegetation may sub- (unspecified) gellei-a of grebes may have been known from ject them iilcidentally to parasitcs with land-based life cycles. the mid- to late Cretaceous. These genera are presumably This may increase the parasite load of the grebes but is, of ones that are now considered not to be grebes but part of course, a dead end in the life cycle of the involved parasite. the early radiation that rcsltlted in the Hesperornithiformes. Grebes rarely come in physical contact with other birds or Hence, the radiation of grebcs came after the breakup of their nests in situations in which exchange of external para- Gondwanaland, on which Stock based much of his analysis. sites might occur. Therefore, the crossover of these parasites The twenty-one Rcccnt grebe species have been divided from other species of birds to grebes nlust be very rare, and among six genera (Storcr 1979). Since the publication of the known ectoparasitc fauna of grebes is correspondingly that list, a twenty first spccies, Aach,rt~ofihorusclarltii, has been low in species. split from A. occirlenlali~ (American Ornithologists' Union Some characteristics and adaptations of intermediate hosts. 1985). A seveirth genus, I-'otlicc;j)horzcs,has been proposed by What makes a suitable intermediate host also needs to be Boclle 1 Aslzi (I994) for what was previously called IJodicups major considercd. Many first intermediate hosts of helminths be- I think this proposal is justified on the basis of both come infected by taking in eggs of the parasites. This may be niorpliological and behavioral grounds detailed in Sanders by eating the eggs, in which case, the eggs must be able to (1967) and Storer (1963a), and I LISC it here. The differcnccs pass through the mouth and without damage. For example, Table 1. The Distribution of Grebe Species. - Continent or major islancl Total species 9 ((iE) ti (3E) 5 (OE) 3(OE) 3(2E) 3(2E) 4(1E) Total gcncra 5 (2E) 4(1E) 2 (OE) 2 (OE) 1 (OF.) 3 (OE) 3 (OE) + = present. - = abscnc. E = enclcmic. " = extinct or cxtil.patcd. + recently colonizetl among the insccts, almost all Iicrniptera obtain their food vae that can develop in it. In turn, thc size of the infcctive by sucliing plant or animal juices througll fine, stra~v-like stage can affect the length of'time needcd Sor the parasitc to beaks which arc unsuitable for taliing in parasite eggs. attain maturity in the deiinitivc host and/or the ultimate size I-lowcvcr, ~licmbcrsof one family of hcrnipterans, the water of the adult. The biology of an intermediate host can affect boatmcn (Corixidae), have a simple mouth opcning and feed its abundance. EIcrbivores and other small sl~ccieslilie de- by sweeping small objccts into it with their brush-like forelegs tritus fecders near the base of the PI-cdationtriangle arc more (GriSSith 1915). This n~cthoclof f'eeding has rnade it possiblc numerous than prcdators near the apex, hence arc more likely lor then1 to ingest eggs ot'the cestodc, Talria bir~mis.I-Iowever, to be eaten, and in greater numbers, by a prospectivc defini- at lcast some corixids possess a crushing "masticator," which, tive or paratenic host. On the other hand, largcr predatory if present in Sigartc, intermediate hosts of' T /)ir(:mis, must be intermccliate hosts arc usually scarcer but may contain larger passccl without damage to the eggs. Most othcr members of and/or more larvae. The trade-offs between these diffcrences can be exemplified by the arnabiliid tapeworms, Tatrin 6iremi.s the Family Anlabiliidae to which Talricc belongs, have nymphs. . of dragonflies and damselflies (Odonata) as interrncdiate and Schistota~ninlunuicirrus. Thc former is a small species, hosts, and it lias been suggcstcd by Boertje (1974) that, in whose intermediate hosts al-ewater boatmen, abundant, small, thc nymph ofthe dragonfly, Anaxjunius, eggs oSSclzi.slotaen,ia algal or detritus feeding hemipterans, whereas the latter's lenr~icirncsare swept into the intestine by action of the cloaca1 intermediate hosts are the predacious nymphs of the very gills. large dragonfly, Anax junius. Taln~rbit-emi.r is found in very 1,arval scl~istosorrrescntcr hosts by dircct penetration of' large numbers (up to several thousand) in a single Eared thc skin. Obviously, the host's skin must be pciletrable by Grcbe (Stock & Holmes 1987b),whereas S. lenuicirrusis found tlic larva, anel the internal environment of the host must be in much smaller numbers (up to 36) in a Pied-billed Grcbe, compatible Sor the schistosomes to mature. PodilymOus podiceps (Boei-tje 1974). It shol~lclbe clcar that the size of a last intermediate host Although no further development of the larval helminths may dctcrmine the maximum size of' the infective stage- of occurs in paratcnic hosts, these hosts are important in col- the parasite and/or the number of individual parasite lar- lecting numbers of the infcctive stages of parasites. In this 4 MIX.P~JHI . Mus. zoo^.. way definitive hosts may get larger numbers of the parasites cies of' prey reported taken by each species of' grebe. Both than they lnight by feeding directly 011 small internlediatc lists include the names of numerous species of animals. In hosts. The intern~ediatehosts of' many l-relminthsare copepods, the various sources used, these anir~lalsrnay be identified to ostl-acods and cladocerans, wliich rnay be too small to be taken, species, genus, family, or merely a higher group. Because of' at least frequently, by grebes. However, when these small crus- this disparity in the level to which these animals have been taceans are taken by snails, fishes, or other paratenic hosts identified and the need to assemble records for all species that are more often taken by grebes, the chances of a grebe's of any genus, family, or higher group, it has been necessary becoming infected bccornc much greater. For example, the to establish a system of classification that can be used con- tapeworm, D%cmnotn(~nincoro~rc~la, prest~mably infects grebes sistently for these animals. Therefore, in order to make com- when they eat snails, which in turn, cat the intermediate l-rosts, parisons between prey of the birds and intermediate and copepodsand ostracods (McDonald 1969; Kyzhikov rl nl. 1985). paratenic hosts of parasites, I have given, as Car as possible, This parasite is a specialist on waterfowl which, unlike grebes, genus, family, and two higher categories for each species. have straining mechanisms in the bill and eat lal-ge numbers (In a few instances in which the lists of prey species and in- of small crustaceans. Snails, acting as parate~iichosts for tliis termediate hosts from genera are very long, only the name pal-asite, make them available to birds like grebes that take of the genus may be given.) To distinguish the levels of clas- larger prey and thus increase the number of possible definitive sification, the nanlc of the highest group is in bold face, the hosts for the parasite, as well as parasites for the grebes. next highest in capital lctters, the family nanlc is in large This idea can be used in seeking unknown intermediate and slnall capital lctters, and the genus and species are in hosts of'parasites. For example, if a fish-eating grebe is found italics. In a few instances, such as the suborders of Odonata, to harbor a parasite whose intermediate l-rosts are known to subgroups are given in plain text. be s~nallcrustaceans, one might look for fislirs as pal-atenic What are given as the two highest groups depends to a 11osts. large extent on the importance of the members of the group The role of anadronlous and catadromous fishes in carrying as hosts and/or prey. Therefore, above the family level, groups inkctive stages of fresh-water parasites to marine hosts and have been chosen largely on the basis of the number of spe- UZCP71~1-~sn does not appear to l~avcreceived much attention. cies involved and the habits of members of the group that MTl-rilc this rnay of'ten be a drad end for the parasite, it rnay may affect their availability to grebes using different forag- be a significant cause of parasitisni for the host. On the other ing techniques. Thus, phylum and class are used for the an- hand, birds like Inany grebes, that breed on fresh water but nelid worms, relatively few of which arc involved, whereas migrate to salt waters f'or the winter, may be important in class and 01-der are used for the arthropods and mollusks, spreading parasites to stopovers on fresh waters enroute to wliich are the two most important groups of intermediate and from the breeding gro~~nds. hosts. Above the family level, most vertebrates arc listed only Purposes. The purposes of this work are h,to prepare a by class, exceptions are made in the amphibians and rep- list of the species of both the internal and external meta- tiles, in which orders arc used, and the fishes (all teleosts, zoan parasites of grebes, with information on their distribc~- except for a few lampreys) are listed only to family because tion, location within or 011 the host, lif'c cycles, including grebes presumably select fishes on the basis of size and avail- lznown intermediate and paratenic hosts, and dcgrcc of ability. For ease in reading, English names are used for higher specificity for grebes as hosts; second, to prepare a list of the groups for which the English group name is synonymous with prey species of grebes for colnparison with the lists of' and derived from the Latin one (e.g., amphipods for intermediate hosts of' the parasites and to establish a data Amphipoda). This has not been done for the orders of in- base to which new material may be added as it becolnes avail- sects because some, like the Hymenoptera, consist of several able; m,to try to determine more specifically how grebes' groups with different English names. For the purposes of parasite faunas may be related to the birds' morphology and this work, consistency in which levels among the higher taxo- aql~aticway of life, including their food and foraging methods, nomic ranks are used is immaterial, whereas consistency be- their peculiar nesting habits, and the annual moves of many tween the two data sets in the nomenclature of the animals of' them to and from fresh-water breeding habitats and salt- and in which higher groups are used is essential for the corn- water winter quarters. Other questions such as the degree of puter analysis. host spccificity, the possible coevolution of groups of para- As groups of animals become better known, their classifi- site species with tl-rose of the hosts, and possible clues to the cation and nomenclature change. Compilers of works on pl-rylogeneticrelationships of grebes with those of other groups parasitology often list the hosts of a species of parasite from of birds through similarity of their parasite faunas, may be the literature without making certain that each host is al- considered. Finally, because the point of view of an ornitholo- ways listed tinder the same name. As a consequence, thc same gist differs from that of a parasitologist, suggestions for fur- host often appears in this literature under several names. ther work will be made. The same problem arises in lists of the prey species of a de- Methods. This review is based on the literature, much of finitive host. For this reason, I have found it necessary to which has been published in languages, many of them Slavic, standardize the nomenclature and classification of all the ~mhmiliarto me. Furthermore, some are in obscure works, animals mentioned in tliis work in order to make computer- which l-rave not been available on interlibrary loan. There- based analyses possible. This standardization has been both fore, I rnay l-rave missed some host records. I hope not many. tedious and to a certain extent arbitrary. Two major daca sets have been assembled: a list of the spe- In checking synonymies and assigning the Samilies and other cies of parasites reported from grebes and a list of the spe- higher categories to which genera belong, I have used Vaugl-rt (1 989) Ihl-the niollt~slis;und Robins al. (1991) and Eschnneycr and the first-stage larva reaches the first intermediate host is 8c Bailey (1990) for the fishes. For assistance in tlne systematics the onc designated. ol'othcr gl-oups, 1 have relied on help From many collcagues E. Known interlnediate and paratenic hosts. ;~clinowlctlgedclsewherc (p. 65 Acknowledgments). Specialists F. The degree of host specificity of the parasite. As defined on the va~.iot~sgroups oS parasites have been especially 1ielpPul in Hoberg (1986), "host specificity refers to tlie plienom- in correcting errors in the taxonomy and nornenclatur-c of enon in which specics of helniintlls are li~llitedin distribu- the groups in which they specialize. In sornc instances, tion to phylogenetically related hosts." However, It should especially w11c1.c a~tthoriticsdisagree, I have had to malie be noted that host specificity tntlsc be decoupled from co- itrbitrary clccisions but have tried to indicate divergent speciation. (See Hoberg ~t al. 1997 and references therein.) opinions. Because morc than a few grcbc parasites arc known only from Two subfannilics of aquatic insects 1)elonging to primarily the original description or a very few collections, becaltse terrestrial fa'amilics (the Donaciinac of the Chrysornelidae little or nothing is known about the rates or intensities of [Colcoptcra] and the Nymph~~linaeof tlne Pyralidae [I.epi- infection by most grebe parasites, and because most of the tloptcra] arc listed srp;\rately and the other members of the species of parasites that arc well str~dicdarc fount1 to infect I'ormcr arc listcd as "<:hryso~nelidae,except Donaciinae." This more than one grebe species or genlls, I have devised the is l~sefi~lin indicating tlie greater availability of members of following classification which I think best suits the present thcsr s~~l)l',~~r~iliesto fc)raging gl-cbcs and their possible use situation. It consists of six degrees of increasing specificity: 21s int~rmcdiat~hosts for parasites of aclr~aticbirds. 0. Incidental or cxpcri~ncntali~lfcctio~ls, 01- immatl~r-c stages The list for each major group of parasites is prefaced by a found but specics is not known to rnatrrre in grebes. 1. bricl' dcsc~.iptionof the biology of the grol~pprimarily Soor Generalist, species of' parasitcs that is found commonly in the I,cnc.l'it ol' 11on-parasitologists. morc than one taxonomic group. 2. Specialist in other In the lists ofhclminth parasites, I have included as much group(s), rare or occasional in grebes. 3. Specialist in grebes, of the Sollowing informatio~las possible for each species: r-are or ~lnknownin otlier groups. 4. Known only from type A. The ctu.rcntly recognized name for the species of grebes (grebe) host. 5. Known only from the original description. known lo I)e parasitized. Subspecific names arc ~tsl~allyomitted. An asterisk opposite the naliie of the parasite indicates tliat This list of grche hosts is not intended as a list of all records it is a grebe specialist (categories 3-5). Beca~~sethe catego- for a givcn I~ost,so usually only one record for each host is ries tend to converge, a consiclerable degree of subjectivity inclt~drd.For a list of ~llcscientific and English names of was necessary in allotting them, and in Inany cases queries grcl)es and synonyms commonly used in tlie parasitological were added. This was often the case with category 5, when I literature, scc below (11. 6). found only the original dcscription but could not be certain In par;~sitolohy,it is the practice to list the describer's name that no f1~rthcrcollections had bccn reported. (For the few I'ollowetl by a cotlnna and the year in which description was instances in which grebes act as intermediate hosts, pt~l~lishccl.I llave followed this convention for original de- information on specificity is not included.) This was also the scriptions, ;~ltlno~~gl~I have not 11sct1 commas between the case in category 2, in which itwas often impossible to determine name ol' an at~tliorand datc of publication of other refer- whether a parasite which was for~ndto he common in a group ences cited. I have not listcd in the 1,iteratul-e Cited papers of birds was also specilic to that group. A special case is that in whicl~origin;~l tlescriptio~ls were given unless inlormation of1'elecilu.s Julicneatra~wlnichis confined to coots and 91-ebcs. on hosts othcr tinan the type host or infot-mation on the life Because it is probably that this parasite originated on the cycle ofthe parasite is included. Thus all rcSerctlces in which former and was later transferred to grebes when its intcrme- 111crc is no comma between the narne (s) of the a~~thot-(s) diate louse host crossed over to grebes, it is placed in category ant1 thc datc are included it1 the literature cited. 2? 13. The location within the bocly of the definitive hosts (for G. Freqllcntly used synonyms of the name of tlne pat-asite, tlic species of parasite 21s a wholc) . especially those 11sed in records of the parasite from grebes. (:. Coti~incntsI'rorn which the species of'parasite is known When life-history infor~nationof a species of parasite is (I'rom all hosts). Continents are msed rather than unknown, information inferved from a related species, fol- zoogeographic rcgio~tsbccatlsc most grcbc specics either lowed by a ql~cstioilmark, may be inclttdcd. Some parasites migt'atc fI.otn onc such region to a~iotlieror are resident in known to have intcr~nctliatchosts in fi-csh water are known morc tli;ln one region. Matlagascar and New Zcaland arc added to infect strictly marine birds sttch as auks. These birds prc- to tllc list of continents because each has one or more ell- sumably obtain infections fi-orn anadrornous fishes (e.~.,some tlen~icspecies of grebe. salrnonicls and smelt). In sllch cases, SW is also givcn with a 1). Wl1c:tllcr the life cycle of the parasite is based on fresh question mark. watcr (FIAT), salt water (SMI), brackish watcr (RW), 01-, in a In the accounts of several species of parasites which have Sew c;~scs,is tcr~.cstrial(T). This may be complicated in in- unusual life cycles, Inore dccailed accounts are presented to st;tnccs in which the last (;.(,., i~ll'cctivc)ir~tct-rnetliatc host givc an idca of the diversity of thcsc cycles found among the or :r pa~xtenichost m;~y move fr-om f~-eshto salt watcr like parasites of grebes. the young of anadromous lishes (some salmonids and smelts) Genera and species are listed alphabetically within each or ~i(.(,71or.\(~,like the young of catadromous fishes (e.g.., eels), family. The names of sl~bfamiliesand subgenera arc often or 111ixy live in both habits (e.g., some killifishes [fi~ndukus] omitted. ant1 sonre sticlzlehaclzs [(;(~.s/~ro.tt~zr.sand Prrn,gili,us]). I11 such The lists of ectopar-asites include the nanics of the para- cases, tllc 11;lbitat in wliicll thc parasite's egg is deposited site and of the hosts and the continents from which the para- (i MI\<.PLIHL. MUS. ZOOL., UNIV. MICII., No. 188 sites arc kilow~i. only for the IHoary-llcaded (;rrbe and the New Zcala~ld In t11c lists of prey of grchcs, tl~rspccies rccordctl are pl-e- Dabchick, once also includetl in I'odicc.f,.s. The Short-winged scntcd in the same spstcln ol'classilication as that rlsctl in the Grebe, Rollnndim ~~~ic.ro/)lrrrrwas fornicrly placed in t11c intcrmcdiatc hosts. This hiis been do~leto permit parallel nionotypic gcilus Cntropelr?ia, and the ~noirotypicgenlts search and cornpal-ison by computer. I,%rnnotJylr.\proposrd for 'Ihchybnplus clorriinicus has not been Parasites ~iotidentificcl to ~ianledspecies, those found in accepted. Tlie nallle, Potlirrp.~ccrs/~icu.\, was widely rlsed for I! grebes not idc~ltil'iedto specics, those not known to mature nigricollis ur~tilit was placed on the Ofiicial Intlex of'Kcjcctcd in grebes, and those resulting f'r-om experiments or incideri- and Invalitl Names by the Intel-national <:om~nissionon Zoo- tal i~~f'ections(e.g., in Zoos) are brackctetl on tlle lists and logical Nomenclature (I. (:. Z. N., 1955). Aoclr~no~)honr.sclnrltii arc not inclutled in the records 11scc1in the analyses. was not I-ecognirecl as a distinct sprcirs until 1985, hence Specimens ~.cportedill the litcraturc to 11e in collections rrcorcls for A. o~cid~17L~li~pres~~~nably may include soine fi-om of thc U. S. National Mt~scu~ii(USNM) and the U. S. Drpt. A. clnrltii. The Great Grebe (fol-mcrly J'odicc,Iis major) has re- of Agricultul-e (USllA) arc now in the U. S. National Pal-asite cently been placed in a monotypic genus (1'odicc~~)hovu.v)by (:ollvction (USNPC) , Agricnltural Kcsearch Service, Beltsvillc, Bochenski (1994),whirl1 I considr~-valid, altl~oughI (lo not Marylantl. A recent accoluit of thr conlplcx histol-y of these accept Bochenski's propos;ll to elevate Po(licc~/).sgri.s(~genc~ collections can be found in 1.iclrtcnfels el nl. (1992). As is hollio~lliito specific rank for reasons I have presented else- customary ill I-efcrring to this material, it is listed by the ac- whcrc (Storel- 1996). The generic nainc, Colj~mfiu.s,was uscd cession number. Parasite spccirncns in the H. W. Manter for the loons ((;tr?~rn) in the Old World literature a11d fhr Lal)oratory, Lincoln, Nebraska, are referred to as I-lMiM with the grebcs (I-'odicr~~.c)ill that of Illr New Miorld until 1972, tlicir accession nmnl1ei-s. Speci~ncnsoP1)irds in the collections when Colyrt~huswas placed on the Official Index of Rcjcctcd of tllc U~iivel-sityof Michigan Musellm of Zoology itre referred anel Invalicl (;e~iericNames in Zoology by the International to as UMMZ with their catalogue nunihers. Co~riniissionon Zoological No11ienclatn1-e(I. C:. Z. N., 1972). To facilitate searching and analyses, the basic data on each It is therefore difficult or inipossi1)lr LO know which gro1111 named parasite species have been pnt into ;r computrr- data was nleant by (:olymhu.s before that date 11nles.s a specific Iiame basc. Thcsc data inclndc, where kriown, thc class, order, and was given with it. Thc only specific Iiamr which is in the syn- family, geogfi~plricrange, habitat in wliicli the par;-lsitc is o~ly~nyof both grebes :uid loons is crnlicc~(-us) wliich has trans~ilitlcd(salt, fi-esh, or brackisli water), clegl-ec of host been applied to the Horned GI-ebe,as well as to the Arctic speciticity, site ofinfkction in tlic grrl)e host, and intermediate, Loon. Althol~ghthe generic narnc uscd wit11 it usually indi- par-atcnic, and grebe hosts ol'cach parasite species. A list of cates to which grollp the bird bclongs, when listcd as a spe- thc known prey species of each grebe species is also in the cies olColynzbit.~, it cannot always idrntifieci to order. In some data base. Separate records for each specics of parasite and insta~icesin which (;olymbzrs was used withol~ta specific riame, grebe havc been crcatcd and ~~ianip~~lated~isillgthe PI-ogr-am FilcMalter Pro (Claris Gorp. 1994). Tl~isis available on the I have tricd to dcter~riin?whether it rcfc'crred to Podicc$s or Cn71icc. 'This hanlca~it listi~ig a Pew spcrics known fio~nlooris web at 111 recent years extensive work on the systcrnatics of' sule, (or in the case of the Plagiorchioids, the egbr is' eaten Iicl~ninthshas appeared, but much still rernains to bc done. and the miraciclia hatch in the first intermediate host). The Son~e30,000 species of l~elmintlislia\~e been described, yet rniracidia arc minute, ovoid objects, which swim by means of several t1io~1s;rncIprobably remain to bc nanrecl. Many of tlie cilia. Free-living ones penetrate the first intermcdiatc host, tlcscril)cd species at-c k~iowtiSt-om a single collection and/ a 111o1111sk,almost always a snail, in which asexual I-eproduc- or f'rom poorly prcservcd material, so sornc rrlay provc to be tion in larval stages (mothcr and dac~ghtersporocysts and/ synonymous with better-known species. In addition, the life or mother and daughter rcdia), occurs. Like the adults, re- cyclcs of many species remain to be worked o11t. dia have digestive tracts and feed actively on the host's tis- Bccatrsc or' the importance of helminth parasites to tlie slle. This asexllal reproduction results in the production of health of'hu~nansand their domestic anti game animals, Par large numbers of the next larval stage, the ccrcaria. Altliough more time and mot1c.y has been expended on their study sotrle cerc:at-iae encyst on objects (oftcn the shell or opercu- than on that of wild animals and birds. In tl~ecase of grebes 111m of a snail, or at least in some notocotylids, plants) in tlie and otl~erf'ish-eating birds, much oP the work on parasites water, nlost havc tails and swim abo11t crtltil they are eaten by has I~cc~ltlonc in castct-11Ellrope, where there are imporian~ ot- penetrate a second intermediate host. This is oftcn a crus- f'rcsh-water fishc~.ics.The rcsults of many of' these studies tacean, insect lat.va, or fish, but sometimes a second, or the have been p~~blislicdin Slavic langl~ages.The inability of same snail, or in the case of' Strigea falconis and some of its Inany pi~rasitologistso~~tsidc ol'this region to read Sl;rvic Ian- relatives, an amphibian la~.va.In the second intermediate host g11;rgcs and the diPficulty of obtaining sonic of these the ccrcaria encysts and transforms into a metacercaria, which pul)lications have 1.csr11tcdin less than optilnal communication is like a small copy of tlie adr~lt,except that the reproductive between parasitologists in cliffcrcnt regions, and all too of'ten systems are incompletely developed or in an inirrlature state. Western pal-asitologists have ignored rnucli of tllc important The delinitive host acquires the parasite by eating the sec- worli tlonc in the Pol-nler Soviet liepublics. Poor ond intcrmcdiatc host or an ol?jcct on which the cercariae corrimunication also has ~nadeit difictrlt or impossible to encyst. Most adult flr~krsare folrnd in the host's digestive assc~nblctypes and othcl. materials nccclcd for thorough tract or appendages to it, srlch as the I~mgs,liver, bile duct, t.cvisions of "difficult" groups. and Bursa of Fabricius, but some arc found in the blood ves- I'rogrcss in the study of grebe parasites also Ilas bccn harn- sels, coelom, air sacs, head cavities, or cyes. Strigcids havc pc1.ec1Ily thc cliSSicr11ty of ltecping these birds in captivity tllc most complex life cycle of tlie digenes, which itlvolvcs a ((:;rlleg;rri 1956), which increases the problems of making special (mesocercarial) larval stage, and a third intermcdi- cxpcrinlcntal stlrdics of the parasites' lice cyclcs. ate host (See Fig. 2, p. 15.). Approximately one l~all'ofthe species of tligcilcs rcl~orted PI..\NOIIHJI)AI.(HC~~SOIIIII II~~IO~~I~S, [itlso in l'lnrrorl~is c.orrr(,u.\ from grebes appear to hc spccialists ill that group (;.I>., gl-ebes and P. j+~lnrrorl~isSzitlat 19321) in which first t\ro larval arc the 11sual or only linown definitive hosts). Of lhcsc spc- stages ;we louritl. (:on1111011in ;i~~;~tids,one ~rccot-deach in Po(/ilyirrbirsf~otlicef).\,C~f)~ll(i, 2nd Hirrrrrr~fof~r~c(2). I.ifc cialists lnoi-e than half are I-c:ported fl-om only one species cyclc in Stunkard (1 934) ant1 (as "7$f~/~loc.o(~lunic:yrnbi~irn, ' of grebe and many, known only horn the original descrip- SI-cckum;~r;ln& Pctcl- 1973). Also, unc1c1- what is tion, may prove synonymotls wit11 other species. It is thcrcforc probably ;I synonyrn, 7: ti.touii (firle S. (:. Scltell, pess. likely that the ntuilber ol'grel~especialists will prove srnaller comm.), by Szidat (1932) and McDonald (1969: 127- than now recognized wllell the sprcies of parasites are better 128). C,~mbiumis ;I noun in apposition Jld(,Ya~nagtlti (1971). known. It is also likely that when more collections of the . . parasites arc nradc, fcwcr species will be know^^ to parasitize Iransroc~lrrrr~oc.ulcrrm (I I), I(:.r,\r.ui /lnv~.sc.rrrs), I'~~C.II.III)AP:(Pocrilin [ "Lrbisi~~a" ] ~-~ticr~la/a, Pl~:\~ORblu.\h(An7.5 u.5, 1)7sculi/er [ "Spimlfnn " ] , (;jli-nitlir~, I'oecilicr [ "/Molli~n~\in"1 lcitil,innn), Uhl~~lu,~( IJmbrti limi), Plar~orbis), VI\I.VI\III),\I~ ( Vnlvaln) , VI\JIPAUII)I\L( Vi~~zj)~rus cllcysting on the gill Silamcnts (Beaver 1941). [ "l'~ilitrlii~n"I); then GASTIIOPODS, Bu~.l.rn'~u,\e *l TROI'OI)S, Rr ~II~NII~.-\I;.(Rillry~rirr "Ritlimris " .slrinlrtli~s, hosts fi-orn McDonald (lW9: lor. fit.). Generalist (I), Ifirlrohioi(l(,.s "/'arc~/ossantlrrs" rnn~rchortric.u.s)then fishes: colnlnon in watcrtowl and shol-cbirds, rarc or inci- I',AGI (Vilil~i/rcrr-lrs["l'ciltrtlirrcr"] rriuipnrrr5 Y:lrni~guti 1971),then? FW? S. Amel-. (AI-gcntina) Internled. hosts, snails? then, Generalist (I), ~.;rrcin gl-cbcs, also in al~oschirdsand lislles? ducks. A4t,tor-rlric clt~nti/:~rlnttrt(Rudolphi, 1802) .Yili/:hirroclo~rroi~r/pl:rrr?(Lir~rr~ (Mclilis in (:~.eplin,1846) In Pucli/:t~pho~rrcinnjor (Torres (11 (11. 1982, vouclrcr in I'otlic.c~f),s~r.\~:~'oncr,P /:r-i.\/ot~is (Bitt~lcr & Sprchn 1928). USNPC No. 076820.00), 1'. iiig~-i/:olli.s(I tr;~ct.S\l'? S. ,b\rn. Intcr.mctl, ho.;ts?] Sm;lll intestine. FlZ? Asia. Intcrnicd. hosts. snails? tlicn? l'(tt(igi/i~r1riIolrt1.s (K~~tlolplii,1819) I? hrr7lircrrrtln Isliii is ;I s!rnoriym~/i/lrYamaguti (1971). 111 7iirhyhnj)tri.c n~/i'r~olli.r(Mc1)on;lld 191i!): 1.56). Small *I'~l(z.vi,q~~rrrlqqornrrlltrrr~r KotlAn. 1922 intcstinc. 1:\2'. I Iric.io/~rrrrr),(:YI'I:INII)AI. (Ahrnmi.~ hrcrirrn, 11. [ "Blicc-n"] (;I.OSSII,II~NIII),\I,.((~lo\\i~)Ir~~iii~r inel. "l~~~r~~o/)~l~ll/~, " Hrlobd~lln,Hcmrtl(.l,.si\, 7'k(~roinprorr), HIRIII)INII).\I. (Nn~inoj~is),Plsc:lc:ol.~~~n~c (l'icrirolir); mollusks: GASTKOPOI)S, I.~~IN,\I~III.\I:(1.y iirirrii,c~); insects: loin) , S~\l.hlo~ll)hl'.(Co~(,gon IIS n//)rt/n). Grche specialist ODONATA, Anisoptera, AI:S~.IINII),\I.(Ar,.\chiln); 01- fishes: (3). The gr~ir~sl~as bcrn considcrcd a subgenus of l3~1.1~oKII).\I:. (Ni~ini~c./ri~ilu.c), (;()I I II):\L ( (,'ol/r~\),(~YI~I cl-s cal-licl- rccortls of Lliis p;ll.asitc li-~IIIgrrhcs to ;tp- "Uor-i~ohtlclltr," Holohdi~lln,H~rnic.I~[).ri.\), H:\I~RIOI>II),\K ply to 7: /)orlic.i/~intr. (H(/?inOf~i.\[ "Hn(,r~io/~si.\"1 ), Pl~(:l(:Ol.ll)~\l~(Pis~i~~l/i), [ 7:$iod~l/,h? \ glo.\.\oirlc.\( 1111hois, 1 $128) S.\I.ITII)\I< (Sn/i/n, "H~r/)~hdollir'3. ( ;eneralist, conilnolr "(:ol~~mb~rs(isi~trr~i~" W~IS listed in Yalilagllti (1071) as itr ;~n;ttidsand clial-;idriif'orm birds, rare in grebes (I). clcfinitivc I~ostol (;lo.\.todi/~lo~loh~~~irr(=7ylotlrl/1lry.\) [ (;otylur-r~sJlnhrlliforini.\ (Faust , 19 17) glo\coitlrc. Bec;~~~scI cannot lind "trsiir/ic.rts"in tlie recent In Porl~l~rnhrrsporlicr/~c(cxpcl~imcnt;tlly, Campbell 19%). synonymies ofspccilic lialncs oSeitlie~-Cmiinol- hh"~l~.i, Intcstincs. FW. N. Atner. I~ltcrlnrtl.hosts, mollusks: I think this is a Iri/~.ciicc.nlnini 101-the loon, C. rrrr/ic.rrs. CRSTlIOI'OL)S, LY~~IN:\I:II):\I.(I~J~IIIIIOPN), 1'1 ,\N~I~I [ "I(lrr " 1 irlir.c, I,PII~IUCI~S[ "Sq1/cili1r.v " ] rrj)lrnl~r.v.I,, [ ''S''I I~rrcivrrr.c,Sr~rr~linirrv ~r,ythro/)lr/hol~r~~~.(, Tinrn tincei, \'i,nhci I ':.\h,nm 11t " ] ~rimhn),PERCID.\F. (.y/i:ov/rdion [ "~,rtr~o/)nrcr'1 Iirrio/)rrr~i,,S. [ "Id." ] r~ol,qrrz,vi,~),S \I.\IO\II).\F ( (,'orrqconir,t In7~rrrr~/rr.c).D;I~;I from J7;1rnagl~ti(1 971 ). Spcci;llist in I.;I~-i ;~ntl;\lcac, rare in grebes (2). M;~rincbirds such ;IS ;~lcitlsniay obtain tliis parasite fro111 an;lclrornot~s fishes s11cl1;IS smelt (0.vrn~rir.v)or s;llnionids (Snlr~rlinrts). (,'o/,ylrr,.~r.vrnr(ti~r.v Dul~ois 8C Rausch. 19.50 consitlcrcd ;I s~~nony~iih!, Yi~milguti 19.58: and Dl~hois1 !)(i8). ~r~h//r,yoro/,ylrrrrrs/)/n~r~/rn/~r,s (Crcplin. 1825) Szidat, 1928 111 7irrh?hn/)/1rsnr/irollis (Vaido\l;~196 .?a), Potlirr/)s rr'I'.v/~/ir.v (XIIT~:I~II t i 19.58) , I? ci rrri/~~.r,I? n igrirolli,r, ,st rrlr vro/)/r or~i.s orri/lrn/nlis ((;alIiniorc 1964). Rursa Fahricii (most frc- tl11('111ly[(;i~lli~norc 1964]), cloilci~,~-c~tunl. Ii11-gc in- testinc*. F\Z'? Er~r;isi;l.Intcrmcd. hosts? and scc. ;~hovc r~ntlrrI. /)ilaolr~s.(;cncralist (1 ). common in 1,ilri. also in illen, (:r/)/)lrirc, (;nrlin, ctc. (McDon;~ld19(i9:8.3-84). 1)11I)ois(l!lfiX) divided "C. " (= I.) /)l~~rf~/)lrnlrtsinto two s~~l~spccics,(,'. /). rorr11111111i.v~ froni 1~7r11.vn~;yrri/n/?r,~ in X. .~\nic.r:arid the nominate race from Ellr;~si;l. I1nrcro/riipw rnhrrv/cr Szidat, 1928 In 'lirrh,yhn/)/irs ri1Jicol1i.v (\'aidov;\ l!)(i.5). Srn;lll intcs- tin(-. Kr~r;~si;l.N. :\mcr. Fly. lntcrmcd. hosts, mollusks: (;:\STKOPODS, I'I..\soRRII).\F. (r\~~i.vr~.v,ncr/lr,yo~n/)lrnltr~, (;,yrcilrl1tr. I'lnnorhi.v, Sr,q~rrrn/inn).tli~n amphibians: ANUKANS. I{I'F~NII).\F.(Blrfh hr~fo),K\srn.\e (I .sc.or;f,i7r.c,Myoxoc././,I1~1,tr [ "Ac.nn/hocott ro" ] ), (;.\n~n,\~ In Rollrr~~rlicrrolland (Mal-tol-clli11jX8). (:acc;l. FM'?, SW? ( Gtidrcc, Microgcitlrr.c, 1'ollnc.hins [ "Pullnc.hi~r5 "1 ) , (:oI\III):\I: Amcr. Intcrmcd. hosts, mollusks: GASTROPODS, ( ~;o/Jill,\),L~l\l (:\rtr 11 /lror~clo/).s,(d:\~rlofiv [incl . " 12lr.voe~rln/)c,'1 lrrcy-lops, ,l\irro/;yrlo/)v), DI,\I~I,O\III)\K (l)in/)/o~r~rr.s, k;rrdi/r/)tor~~ 11,5), tlicn FW fishes: c.spcci;illy (;o~rr~r)\K, ((;obiti.s tn/>nin, .221nnelrilrr.skrr.vclr~rk~rrlitrchi, .V. .stolir:kni, ,\: $11-cr~rrlri.;lnd ?,V. ~.io~:vnli.s).1,css ol'tcn in (:\~~KINII).\F.(Gobiog01)io. Rnr1)rr.s h~~~rrlryeo/)lrnl~~.r,I,rrrcns/)irrs tlrlin mt 1r.v) . (;enera1 ist ( 1) . nlost conilnon in g~~bcs.I)l~binin;i (19tX) divitlcs 1.i~prIr into Ii\.c species (t~voof\\~liicli arc l~nn;t~ncd)each of ~vl~icliis considcrcd ;I spcci;ilist on a rliff'ercnt group offislics ;ISintcrmcdiittc hosts. Schmidt considers 1,i~prln nlonotypic, with I.. intr.vtin~~li.sthe only species. I.i,q,tln int/>stinrrlis(I,inni\cus, 17.58) In :\rclrmo/)ho~-lcsorcid~~rt~li.~ (Stock & Holnics 1987h), I'o/iil~~nhrtr /)o/iic/j/)~ ( Perez-I'oncc tlc 1,con vt nl. 1992. id \~or~chcrsin LISNP(: Sos. 007859.00, 02I)(i73.00), 'lirch~hrr/)trrt rtrfic.olli\., I'o~lic~/)s~rrritlr.~, I). gri.rr,qrn~ (\,ol~c.lic~.in I'SNP(; No. 079328.00). 1'. cri.rtntrrs. 1) rri,yrirollis. I.;irgc and small intcstincs, kidney (Sliigin 1957). F1V. (:osmopolit;tn. Intcr~ncrl.hosts, crustaceans: (:orl fishes: AN:\RIII~:II~\I)II):\E(Annrlrirhns [SW]),AN(;L~II.I.II),.\E ports from FI4' fishe\ probablv erroneous (McDonald (:I n~lrrillonrr~r~rilln [FMT. STY] ) . ROTI111, \E (Sco/)IrtIrnl?n11s 1969:66S664).Immature stages in mink (~Ifzctl~lnrrrson). "Rlromhrrs"1 rnn.uirnrr.s [STZ']),C;I.C;PEID.\F. ((;lrrprn hnrmlgtrs Common in marinc m;lmmals, rare in cormorants, [SW],C. Ir. /~crllnsi [ "m~mhrn.s"][STV] ), C,o.r.rlr).-\~ herons, mcrganscrs, and other fish-eating birds, in ((;yrn~rocnntlrrtsr~rr~trnlis, i\lyo.roe~phnlrts [ "Cottrrs" ] \vhic11 it is not known to mature.] ~lrrcrclrir.orrris [ST$'], ,\I. [ "C. "1 .scor/)ilts [SW]) , [Cnr?nosonrn ytrrlrnorrtm (Rudolphi, 1802) (:V~:I.~I>.SEUII)~\E( (,~ycIoj)I~rir~ 1irmprr.s [SMr]), CVPRISII)~\E In fod~ceps,prqpnn. Small intestine. SW. Eurasia, N. (Ahrnmis [ "Rliccn " ] 1,jo~rknn[FW] . I,PIIC~.~C?IS[ "I~IIS " ] Amer., S. Amer. Intcrmed. hosts, crustaceans: idrr.v, 7'inen tinrn (n.~Corjnosomn ".rmrrinr" Hoffman AyjPHIPODS, L~SItssrn \F (fonto/)or~10)and second [ 196'71 [n4']), Esoc:rn:\~ (fiox Irrciris [FIIT]). G.-\nln..\~ intermediate hosts, and, probably, paratcnic hosts, (fil~~qintcsnnvngn [SW], Gndir.~[morhrrcr] cnllnrins [SW], milrine and nnadromous or catadromous fishes: (;.\s.r~~uos.~.v.~~>,\~.( I'IItlp'tirr,.s j)~r?r,g-iti~r.r[FTY. SMT]) , I,o.rrn..w. A.~~.vIII In \F (L/\n*q~~//nn?r,prt//n [nv, SMT] ), A~13~ulllln\F (I:'~rrh~l~o/)~r~ci~nl)r-i~r~ [ "0110,s clonhri?l IIS n] [SFV]. I,otn (Alhmnn /)o?rt~cn[FM', SM']), ~OTIIID\F(Scojlhthnlmur lot(r incl. "I,. r~rrl,q(~ri.v" [FW] ), M~u~,rcr~n.\l~(Mncrrtmnils mnxlmu~[SW] ), CI UI'F 11) \t. (Cns/)fnlosnspp. [FW],Clirprn no7rnrz1~lnrrtlin~[SW] ). OI~IIII~IID.\F.( CIrn?/)trrrr.s 1)lneodrs hnrrngrrs [SM'] ) , Covc.nrn-\r ( Chngrr rongrr [SM'] ) , [SW]),OS~IF.KI~.\F. (OP~PI~IS [morrlnx] tirntpx [FIY, S\V], COIIrn \F ((:ottirs nPnrliq, C. hrrhnl~r,I,p/)tocott~rr nrmniirs 0. rjlrrln n rr.s [FW, STV] ) . P~.rnosn-zos.r~r).\~(I,nrnp~tm [Fly. SM'] , ,Ihouocrj)hnlirr qirndnronr~r[SW] , ,\f. rcorj)~tis ,j/r/)onicn [FW,SW] ). Pr.~.rruo~~:c:.rrn.\~(I,io/).srttn g/nrinlis, [SW]), CICIOPI FRII) \! (C?clo/)t~rurIi~rn/)us [SW] ), I'lr~rron~rlrs,j7rsrrs [SU', FW], I? lirntrnder [SW], I? Plnlrssn Esoc 11) \F (I<\o.u Iirc111s[FM']), G \I)rn \E (Clnrlirs [mo?lrirn] [STI'] ) , S \I.\IOSII).\E( Corpgorr ris nlhlrln [F14', RTY]. C. mllnnus [SM'], C;. rnnrror~/)irnltr\[SMT], (; \STFUOSTFII) \F In7wr~tic.s [FW, RM1], OncorIr?nchirs nrrltn [FW, SM'], (G~sI~rortrirsncrrlrnt~rs, Ptrng?t-ilrrr\ p~inptl~rs[both FTY, Snlr~rli~lirsnl/)inrr.s [FW, SM'] . S~ICII.\IID,\E(I,ttmprntrs STY]). LOPIIIII)\F(I,o/)Irlirs j)~scntort~rs[STY]), Ihtn lotn fnhricii [ST4']) , Zo \R(:II).\F-.( Zonrrrs 71irri/)(rrttr[STY] ) . Re- [incl. I>. ~r~rlpnrts][FTV]), O~VFRID\F (Osmrrrrr mordo.~ 1 "drntrx"] [FW, SW], 0. r,brrlnnrr~[FW, SWI, S,brrinc.l~u.\ 1969).Intcstine. FW. Etrrasia, N. A11ic1-.Intel-med. Iiosts, [ "O.s~nc~rtc,s" ] la~rr(~oltr/tt,s[FW, SW1) , PI,I ROI\IYLOI\' I IDAE crustaceans: AMPI3IPODS, G\I\IRI,\KII):\I:(C;ammrrrus (Ccrspiomyzo~twngneri [FW], Lnml)rtra Jllr7iinlili~ [FW] , lac.urlri~),pal-atcnic hosts? (;eneralist (?I), co~n~non l'(~/ro~r~yzonsp. [FW, SW] ) , PL.I-LII nlost con1111o11ill \V;II~I~I'O~VI.( I ) , l I'orrocnocri~cr rrc~ssum(ljeslor~gclra~r~ps, 1824) [ "C,a.slrirnnrgi(lr.c'" ) ), RI.A~~IU;\~(Prril)lnn,rta), DIPTERA, In l'orlirr~f~sg~i.\rg-(,':~/')cn. S~O~I~~ICII,small intcstinc. FW, T. Clrruo~oi\rr~~\e(Clrcrorrorn~cs [ "E7cdipes "I, Critotopuc, 1.lu1-itsia.Intcrmcd. hosts, annelids: OLIGOCIIAE'TES C.'rrlicoides, Polypedilum [ "Poliprdium"], Proclndi,us). [TI, (;r.ossosc:o~.~.:c:~~),\~.( Criodril~is) , LUI~IUKI(:II)I\I' I'aratcnic hosts, fishes: CI UI'EIL),\E(Cn.s~~inlo.src (i\llolobol)hora, l)entlrobcic,tia, Lisr?iia, I?'i.\rnirlln, Rophila, hrashnikovi), CYI~IIINIDAL(R~rtiluc rutil.c~s, Seadintus Oclolnsiclnc) inkctctl, at least cxpcrinicnr;tlly. Corntnorl ~rythrol)l~/lcnlrrtus),GOUIII)I\L (N~ognbi7~s ,flii71inl~lis, N. in ;~ni~tids,rare in grehes (2). mrlanostomctm) , I'ER<:II).ZE(Slizo.\tedion [ "Lircio/~c.rca"] ":l'orrocneclr~r~~)rri(~Io7rgrrm (lhjardin, 1845) lucioprrca). Generalist (1 ). 1,ilc cyclc in Anderson I11 I'odire/).s nrtri/ci,s, typc and only known host. lntcs- (1992). tine. T?. FW? Europe, not rcpor~ctlsince 01-iginaldc- :':T~lr(itn~w~#-1rl)c1?i07ii Sl~igin, 1957 scription (5). Intcrmcd. hosts? Stat~rsin question. In 7i~clryboplusnouneholla71d1ar (Mawson ef nl., 1986), IJorroccrrc.rrm r~f~crrlnl?trn(I.instow, 1899) 7: ruficollis (BaruS Xc ZajiEck 1967), l'oditeps grisegena, 111 I'odict.l,r crrflnlu\ ((:hiriac 1965). Tntcstirrc. FW. Eura- I! cris/n/us, I? nigritollis. Esophagus, provcntriculus. FW? sia, N. Arner., Al'r. Inlcctivc larvac in fishes: C(YIrlo,\e Eurasia, Austl-. Intcrrnrd. hosts, crusracea~~s?Appal-- ( D~//ussp.),CVPI:INII)~\K (C$f~?iniis cccrpio, Pe1rcu.s cullrc~lu.>). erltly conrinrd to grcbcs (3). Placed ill Trr~j~i.tur-11,sby I-lcl-on specialist, 1x1-e in grebes (2). BarrlS Rc %iijit.ck 1967. Order Spirlirida SuperLunily Acllarioidca Subortlc~-(;alnall;tnitra Family Acuariidae S11pcr1':rinily Dracrr~~cr~loideit Subfiimily Acuariinae Mlsr.. PUBL.MUS. ZOOL., UNIV. MI~H., No. 188 (:oc~rnor./"f,herlltso~~IPIo~I~.~ (Crcplin, 1825) Apparently confined to grcbcs (3).C~onsiclcrccl a syno- 111 iLe/'hm,o/fhOrn! oc.cidrt~/nlr.\(<;;lllimol-c 1964 [as (;. 11y1ir of K. rlorrgtt/tr by Smogor~hcvskaya1990. /'irloll(,ij). Potlic.o/)c cllcril,ll\, I! grisc~gc~irn,P c.rrilnl~is,P [Skjnbin,oc./avcr d~c.omto(Solonitsin, 1928) ~rriyic.olli.\.Esophagus. FW, SW. (;os~~iopolitan,except In I'odzcc,ps nci~-il,us,I! rrislnlu,s. l'rovcntricult~s.FW?, SW? S. Airrcn (12eportcd fro111 four genera ofAlcicls by UaruS EUI-asia.Intcrmcd. hosts? Specialist in shorebirds, re- (,/ nl. 1978). Intcrmcd. hosts, crustaceans: AMPHIPODS, pol-ts 1.1-om grebes and passel-il~rbirds i~redverifica- tion. (0) I ( (;nrnmnr.zlc Jnsc.inlli\) , T,\l.~,rnru,\~(Hytcl(,lln trzlercl) . [Sk?lobinoclavo horrlda (Rltdolpl~i,1809) P.~. I ..atenic hosts, fishes: (:o.~I IIIAI: ((:ottr~~sp.), (:VI~RINI- In 7irc.lryhnptut nouccrliollrrncliw (Mawson ~t ol. 1986). I),\IC(iVo/ropi\ hrcd,\o~rriris, Srmo/ilis ntromac.rrlntrrc), I'rovcntriculus. FW?, SW? Eurasia, Cuba, Austr. (;I\SI I 7 Ih~r-onzyzorr,s~~xot.~rl~r/rrr/z (Moore, 1891) = 7: tc..s,sulic/u~71jici~ The basic (aiid prcs~~mablyancestral) life cycle consists of Oosthlrizcn Pc I)avics (1993). an egg, olie or two six-legged stages (prelarva and larva),one , 01- rno~-c(~lsrlally three) ciglit-lcggctl ny~nphalinstars 11irrorn)~zon lin~cclr~~rnSciacchitane, 1963 = 7: coop~rifzrl~ (~~rotoilyn~pll,dcl~tonynlpll, ancl trito~lynlpll),aiitl the adult. Oostll~~izcn( 1993). Viviparity ant1 suppression of' instal-s liavc cvolvecl in some groups, rcacliing an cxtrclnc ill sonic I'or~iisin which tlic lk- ~nalegives birth to matlu-e adl~lts. (:lass Hirutlinc;~ Although mites arc perhaps the most widesprcatl of para- Ortlcr lihync1~obclcllitl;t sitic arthropods, thc n~~mberof species known from grebes F;rmily C;lossil>honiid;rc is small and linlitcd to fol-ms inhabiting tlic nostl-ils (6) and I'I/~c.ohtlrllno~.~~otn (Vcl-I-ill, 1872) fcathcrs (6).This is presumably 21 rcs~~ltof grebes' cxtrc~l~cly On Porlic.c,/~tcrtrri/rc.t (Mool-c 19(54).Found ;~mongthe aquatic habits ant1 linlitcd pliysical contact with otlicr birds Scatllcrs "pitrtly tlistcntlctl cvitli Olootl." FW. N. A~riel-. or places frcqlieiitctl by other birds oil land. Turtle spcci;~list.01lc rccord oil grebes. Presr~~nahly Mites belonging to both tlic orders I'arasitif'orlncs and 1-;11-c01- incidental on w;~tcrhirtls. AcariSormes inhabit tlic riasal passages of grebes. Species of 7'/1rro~1lyyzo11~Oo/jl,rl (M;ll-tli tlg, 1932) 011 7i1c.l1)lh/r/)/ucI-r~firo1li.t (Oosthui7en & E'o~II-ic1985) the pal-asitifor111 Pninily Rhinonyssidae and the acarifi)rm I'n~nily FW. Afr. Ercynctidac have adapted to this habitat. Althoug11 similar ,I .h(,ronzyzo?t "o(;c.f(l~71/(1li.t"(Vex-]-ill, 1874) ill their microhabitat choice, rnitcs 01' these two lineages are On Potli1yrnh11.t/)o//ic.~,/).\ (Sootcr 1937). FW. N. Amcr-. otherwise qr~itcdifferent. Thc rhinonyssids move slowly in (Iowa). This rccord ~,rcsunlal)lyi.\ referal~lcto one the mucus of tlie nasal passages, whereas the ereyneticls are ol llic I'OIII- I-ccogni;lctlspccics of 7%c,rompzo11with two covered with a hydrophobic cuticle and move about actively ;rnnuli I>ctwccn111e 111;1lcand I'c~n;tlcgonopol-cs. (Scc on the s~trl'aceofthis mucus. Rhinonyssids l'eed on host blood Oosthl~izcn& D;lvics 1993.) , , by picrciirg thro~~gllthe mucus inenlbrancs wit11 highly modi- ~/l~rOl/ly~Ol~IP.\JIL~/L~~~III (0. F. Miillel-, 1714) fied ~not~tliparts,Thc fTcding habits of tlie Ereynetidae arc 011 l'odic.o/)c (riclcr/rr.t (M;IIII~1951). FM'. N. Anic~..,F.111-21- sia. unknown, althol~gl~blood is not typically observed in their 7%~romyzo11"/rizoncrr.c." 1);rvics & Oosth11i7c11, 1993 digestive tracts. 011 I'ooo'ih~~~br~s/jotlicc.l,c, l'otllc.c.l,t ntrrilus, I? ,yris(,,ymn, The life llistorirs of'tlie two groups 01' riasal mites also dif- I? 1tig~ico/li.t,~t~~c./tr~io/~Iior~~.s oc.rr~lc~~~/t~/i.t (C;alli~~~orc 1964). [el-, although both are prcsumably vivipal-ous.The rhi~~onyssicls alternate fccdiiig wit11 non-fccding instars. The non-feeding Moore (19(i4),and thc I;tst (withorrt rcfcrcncc. to tlrc larw is followed by a Seeding protonyrnph, a short-lived non- source) I)y Moorr ( 19(i(i).111 11;ts;ll c;lvity. FW. N. Alncn Seeding deutonymph, and thr feeding adult. The intranasal (Albcrr;~).Thcsc specinrcns, orifiinally idcntiIied as Ereynetidae also exhibit life-cycle compression, having a feed- 7: ri~oo'r(Rail-(1, 1863), ;rrc probal,ly rcfcrahlc to this ing larva fhllowcd clircctly by tlic adult. The nymphal stages spccics, I>UI 1 Ilavc I)(-en ~~nableto I'ilid their ~IICI-ca- are represented by layers of c~iticlelaid down during the period bo~~tsso th;tt their. idclltificatio~icould hr cl~ecked. between the larval instar and the molt to the adult. THE MITES (ACAKINA) OF GREBES The rnites associated with feather habitats belong ro tlirec families in tlie order Acarifol-mes, all of which arc believed The Acari (mites and ticks) f'cjrrn a varied group of' small to have arisen fro111 a comiiion, f'cathei--i~~liabiti~igancestor. to very sniall arthropods, typic;~llyclassified into two orders. The qt~ill-wallmites (L,aminosioptidae) are associated witli The nunlbcr of spccics is cstirnatctl in the millions, but only tlic basal part of the feathers. Tlicsc ~r~itcshave been most a Sew have been descrihetl. Approximately one-half the dc- often collected between the sheath and the rachis of' clcvcl- scribed species ofacai-ines are associated witli other animals, oping q~~ills.Because sllcli mites appear trapped, it seems the renlaindcr occl~pyingaliilost every coiiceivahle niche Inore likely that their natural habitat is tlie feather follicle available to snlall arthropods. Sr~clihabitats i~iclutlcsoil, itself. The food of q~~ill-wallmites is ~uikno\vn.Members of dctritt~s,pl211n1 substrates, and both f'resh and salt ~vater.Plant- tlic other two families live between acljacc~itbarbs of feath- crs, often in great numbers. Species in tlie Family Analgidae Ordel- Acariformes tyj~icallyinhabit the plumulacco~rs(downy) barbs of body con- Suborder Trombidiformcs tour feathers and thc basal parts of [light and tail feathers. Supcrf'alr~ilyTyciroitlra Anitlgid mitcs oflen have nlodified hook-like processes on Farnily Ercynctitlac Nasal rnites tltcil- lcgs which enable them to maneuver among these barbs. *iVeoboytlnin eo~rnl~iji~r~ni(Xal-k, 1964 From Podirc;l,\ 11igric0Ilis, typc host, I'odilymbus fiodicei(,.s Species in the I'aniilp l'tiloxenidae, in contrast, inhabit the (Pence 1973), ?nrlrjbnljl~tsnovnehollairtliir~~ (as "f'oclicr/~s s~;~csI~~twce~ithe barbs of the pcnnaccous parts ofthe flight r-r~ficolli.~,"Doml-ow 1991). N. Anicn, Austr. Grebe spe- ant1 tail feathers. These nlites sllow strongly modified mor- cialist (3). pliologic;~laclaptations to this habitat including the elongated, Subol-dcr Sarcoptihrmcs llatteiictl I~otlyand enlarged, s~~ckct--likepretarsi whicll are Superf>mily Ptcl-olichoidca PI-cssed against the barbs to maintain the nlitcs' positions. Farnily l'tiloxenitlae Feathel- mites All l'c:allic~--inhabitingmites exhibit a life cycle only slightly *Ptilox(vr us col~ttthi(Cancstrini, 1878) modilicd fi-o~nthc anccstr;-ll acariforrn pattern. Eggs are gl11ecI From Tirthybr~~~l~r.i-uficollis. ( "Pod~rr$)smi7tor" given as the type host is a synonym.) Eur. (Reports summa- to (i:atl~crsin highly specific locations, ant1 the prelarval inscar ri;.ccl by ljubinin 1956.) Report from Cr~vinnccds con- is 1xtsx'rI it1 the egg. Thc larva two active nymphal instars and fir~nation.Otherwise ltnown only fr-orn thc typc host arc li~llowcdby thc adult. The clcutonympl~alinstar is st~p- (4). Genus confinctl to grebes. prcsscd in these taxa. q:I'liloxr~i~~~mcrjor (Megnin & Tror~cssart,1884) Thc li~odofkatlier mitcs is little known. Snlall projections Fro111 I'odic-c.l,.s o-i.\tnlz~~,type host, P. nrtrilric, P. g).i.,-i.c~gmc~, ol'f'c:~thcr harbulcs have bccn found in tllc digestive tracts of P 11igricol1i.s.Eun (Duhinin 1956). A rcpori from Cor-vrr~ some analgid mites, while algae, f~uigalspores, and other roronr rur~lixon the Volga Delta, where the niite was tlctritus arc also obscrved, cspccially in parasites of aquatic helievecl to have hccn arquir-cd by fccding on the young birds. It seems no st liliely that the major component of thc of f'odie~I)~eii.\li~lu.\ (Dubinill oP. ril.) is [~reslllllab~~ erroneous (Atyco in litt.). The name of this mite diet is the oil with which birds dress their feathers. Recalrse (spcllcd "maior" in older literature, Atyco in litt.) also I'catllcr mitcs often occur in very high poprllation density, it has appeared in the literature as P. "miriory," evideritly is ~nilikclytliat most grolrps oP external, feather-ii~ll>~bitir~g a ~rarlslileralionfrom Russian (B. O(:onnor-, pel-s. mitcs arc in any way detri~ncntalto their hosts. corr~n~.)Grel~e specialist (5). 1 am n111cIi indebted to Barry M. OConnor For rewriting *Ptilox~nus sp. ant1 expanding the above account to inclnde much informa- From IIP~ILIM(I~I~OT~I~sp., (undescribetl spccies Univ. tion that is not gc~lcrallyavaila1,le. RIA'S. Michigan Mus. Zool.). The classii'ication of the fcatlicr miles is that of Gaud 8c "Sclrizrirolirlrrrs rlrgn7ts (?erny, 1969 Fro111 7irclryb(rj~/i~~ilorninict~r typc host, I'ndi!)'~~th~~.c~~~Iicr~~).~ Atyco 1996. (W. T. Atyco, pcrs. cornm.). N. Amen ((:uba), S. Amen 01-clcl-l';u-asili1'o1-mcs GI-cbrsprcialisl (5). Suborder Mcsostigmaca Supcrfarnily Analgoitlca S~~l~c~'limilyLjcrmanyssoiclca [Family Psorop~oiditlaeFrather mites] 1';trnily Rhinonyssidac Nas;rl niilcs. [Mt~algoidr.\( "Mpsalgcs") oscziiuin (Koch, 1810) Tl~cspccics 01' this I;umily ;rrc quite variable. This has Report horu 7iich)lhnl~tw~uficollis (Gaud in Dolfuss 1961) lctl lo considcl.;~blcspliiiing, which has been countereti is presumably ;rn error-, the type host of Musnlgoidrt by ~nucliIuniping. To clatc, there is no expel-irncnral occinurn is ibfotncillo nlbn and the genus i\4c,scrlgozde, is cvidencc ofnon-gcnciir variation, so, instead of whole- ell..uactcristic -. . of' passerine birds. Mcmbcrs of thc gc- sitlc lumping, 1 ;rm recognizing spccies abort1 which nus iVlesnlgrs a]-e known only fi-om thc Buccl-otidac.] tlicrc has been concrovcrsy OII tl~cgl-ouncls that this ["Coljnisu.\ sp. " reported 1'1-om 7: ~-r~ficollz.rby Gaud Inay provide morc inlormation. Pence (1975) provides (in Doll'uss 1961) is a nomcn nudumJid~Atyeoin lit/.] tlsclill ltcys and spccics, ;u~dhost lists for North hncrican Family Lanlinosioptidae Quill-wall nlitcs lol-ms. *Podiri/~cclico/~f~cmmrricnnu: Lombcrt, I " Coly ttihtis" [=Tnrltyhrr~~t~i.s]riiflcol1i.s cnprnsis by may also be a potential intermediate host for a greater number Shchcrbininn (1966)pres~unably rcl'ci-s to A. runrin,n/zrs. of parasite species as well as individuals. Furthermore, grebes ?I T111lc3. Numbers of Na~ncclSpccies of Parasites Repol.Led from each GI-cbcSpecies. No. Rangc .~ Inc.lryI~~~/~lrts r-rrpt ollic Eurasia, Africa I'orlic.c.l,,grisc~gr~iicr Eurasia, North America I'odi/'f'/l.\ ~fi.\l/l/l/t Eurasia, Ah-., Austl-al.,N. Zcaland I'o(lic.(~/).\11 igric.olli.\ '!: Eu~asia,ilfr., N. and S. America l'oflic.f,/j.\ (~rrr-i/~r.\ Eurasia. Nortlr America North America North and South Atnerica North and Sor~thAmerica South An~erica South America Madagascar New Zeala~id Nortli America (Lakc Atitlin) South Amcl-ica South America (I.akc Jur~in) Soutll Arnerica (Lake Titicaca) So~~tllAmerica Madagascar "'Ir~cludcs3 hel~nintliswhicll occ~~rrcdonly as imrnaturcs canal in the hypotarsus, making it easy to see fi-on1tlic skeleton which are in need of a carefill reassessment before they can wl~cthcrthis muscle is prcscnt or absent. It is present and be used in reconstructing the phylogeny of the group. well dcvclopccl in I'odily~rt~Ous,and the Old World spccics of Unfortunately, no one since has approached this problem, 'li~c./~yhnpl,~i.s,snlall in liolln~~dirc,small or absent in Porlicrphorzcs, and Bocheriski (1994), in his comparative analysis of the and consistently absent in 7ircl~yb(r//t1tsdominic~is, Polioc~phnlu.~ skeletons of grebes, did not rncntion the toe bones. I'oo'icc.l,.c, and i\c~clrrr~oj)I~o~rus.Its f~lnction in moving a single The aquatic existence of grebes is ~vcllreflected in their toe and its presence in I'orli1ymbu.c suggest that its function parasite fauna. To date, 249 named species of helminths (113 is rclatcd tnorc to ma~~c~~vcrabilitythan to rapid swimming. digenes, 86 cestodes, 13 acanthocephalans, and 37 nematodes) Oncc lost in a phyletic line, this muscle has not been have been reported to parasitize birds of this family (Table rcpl;~cctl. I'o(1i~ofisprobably cvolved as a group of fish 2). These figures for the digenes and cestodes combined are specialists, br~tin the l':;lrccl Grebe group (1-1 gr~llnr-chi,P larger than those of any family of aquatic birds listed by Hoberg t,igricollis, I! oc.ci//il(~li.\,and 1-1 Irccz(~no7o~ltii),the first three (1996, Table 2) except the Laridae, a family with approxi- have become specialists on small invet-tebr-ates, whereas 1' mately five times the number of species and with a wider /ntztrno7o,sk%i,which, on the basis of close similarity of plumage geographic and ecologic range than grebes. Compared with and bcliavior pt.ol>ablywas tlerived kom I? o. ,ju,ninen.sis,has the Alcidae, a grot~pof comparable size and diversity, the become a fish cater -- thus presumably having changed its figures for the number of species are approximately three f'ccding specialization three times in the course of its and one half times as great (Table 2). Possible reasons for evoll~tion. the large number of spccics of parasites in grebes include Tlic loss of this Ilexot- ~nusclein 7ircl~yba~1tu.sdwrninicus may the birds' nesting on eutrophic lakes and ponds which pro- llavc rcsultcd from its alrnost complete sympatry with vide a large number and variety of prey species, the grebes' l'odily~rrO~cr,s,which is larger and much Iieaviel--billed and wide geographic range, and, in many of the species, the move adapted lor taking slow-moving, heaxy-bodiecl prey. In this from fresh-water breeding grounds to salt-water wintering casc, bcing smaller, being able to move more rapidly, and areas. This is particularly true in the comparison between having a thinner bill, 7: dominicrc.~would have a competitive the grebes and the alcids, which are marine and forage only advantage over Podilymbusin being able to take faster-moving in salt waters. Comparisons are also hampered by the virtual ancl snlallcr prey. Evidence for this can be seen from the lack or paucity of information on the parasites ofthe South- large numbers oP ants, presumably talien ft-on1 emergent ern-Hemisphere grebes and on grebes on the salt-water win- vegetation or thc water surfixce and the habit of taking flying tering grounds. dragonflies (Storet- 1976). The maxirnmn number of parasite species reported for any A cornpal-ativc stl~clyof'thc f~lnctionalanatomy of the legs grebe is 123 for the Little Grebe ('licchybr~f)[email protected]), whereas ant1 I'ict ol'grcbcs wo~~ldbe a valuable addition to the biolog none have been reported for two South American and one oftlicsc birds, cspcci;~llyif combined with analyses of motion Madagascar endemics (Table 3).This is because few or none picturcs ofthe birds (alien under water. This also ~vouldbe of these birds and those taken on salt water have been inlporcant in assessing cllaractcrs found ill early fbssil grebes, examined for parasites. It is thus probable that the total Figwe (5. Atlaptivc ~xdiatio~~ill thc bill Sorm of grchrs. a. (icncl-alizccl typc. Least Grehe (firhybapltrs dott~rlrirus),111alc (UMMZ no. 90,758) abovc, felnalc (no.100,639) below; b. (:~-~rshingtypc. Pied-billed Grebe (Podilytnb~uspod~c~p~),male (no. 223,028) abovc, Sclnalc (no. 223,031) below; c. Fish-spc;rring type, l la^-k's Grcbc (A~c.hmof~ho~-usrlnrltil), male (no. 158,393) above, lelnalc (no. 158,392) below; d. Insect-picking typc, Silvery (;rebe (Pedicel,, oc.rif)ilnli.\),male (110,157,233); e. Fish-eating typc dcr-ivcd fro111 above, Puna (;~-cbr(Podircps tnc.zu?roru,~kii), Sclnalc (no. 157,236); S. Sn;til specialist, Hoodrd GI-ebc (I'odicep.,~g-tzllnrtloi), nlalc (no. 207,983); g. Large generalist, Shol-t-winged Grebe (Rollntrtlin mrrropl(,m), nlale (no. 157,237); and 11. Fihh-cater, (I'odicepho?-us mnjor), male (no. 204,737). Original dl-awing bylohn Mcgahan. number oSspecies olparasitic helrninths to be found in grebes and is thought to be an adaptation f'or feeding on crayfish, will prove considerably higher, in spite of the likelihood that crabs, and other hard-bodied animals (Zusi & Storer 1969). sonic of the little-known nanlcd species will be found to be The opposite extreme is the sharply pointed bills of the synonylllous with better-known ones. Western and Clark's grebes (A~c.h,mof)horus),which presumably Bill morphology and parasite faunas. Wit11 few exceptions, evolved in connection with the spearing s~iecllanismthat these bill shape ill grebes is basically si~nilar,but within this gen- birds use in obtaining fish (Storer & Nrlcchterlein 1992). eral shape there are numerous variations in proportions Another variant is the broader bill with more upturned man- (Figure 6). Longer, inore slender bills are associated with dible found in the Eared Grebe and its South American rela- catching and holding Sishes, whereas shorter bills are asso- tive, tlie Silvery Grebe (I? occipitnlis),wllicll specialize on small ciatetl with obtaining more slowly-moving prey (Fjeldsd, invertebrates. The swallowing mechanism of tlie latter spe- 1982b).That many of' these difSerenccs arc results of' ecological cies has been analyzed by Fjeldsd (198 1 a), who Sound that cllaracter displacement between sy~npatricpopulations of in manipulating the prey, the birds press the the large, fleshy grebes has been shown convincingly in detail by Fjclcls%(1983). tongue against the roof of the niouth. Mahoney & Jehl (1985) One extreme in bill Sor~nis fonnd iii the Pied-billed and suggest that in the similarly large-tongued Eared Grebe, this Atitlkn grebcs (Pon'ilyn~bus).In this genns the bill is very deep motion squeezes water from around the prey before it is swal- prey, and the fact that many of the grebes' parasites share lowccl. On Mono Lake and similar bodies of highly saline several spccics of grebe hosts appear to negate likelihood water to wllicll t11cse grebes move ior molting and/or win- that a similar situation occurs in any grebe species. tering, this must reduce the amount of salt ingested by feed- At least on the grebes' breeding grounds, one prey spc- ing birtls. The Hooded Grche (Porlic~psgallardoi) has a simi- cies rnay be abundant for a brief period while another bc- lar but broader and heavier bill and feeds to a large extent comes scarce. Such fluctuations necessitate the ability to switch 011 snails (Storcr 1982a; Fjeldsi 1986). In spite of the consid- from one kind of prey to another. For this, a generalized form erable variation in proportions of tlie bill among grebes, the oPbill would be advantageous. The eutl-ophicbodies of fresh diet of all spccics consists ofa wide varicty of prey types (pp. water on which grebes spend rnllcll of the year are rich in 37-41). Sexual dirnorphisni in bill size is a characteristic of the amount and variety of prey. Ilere, again, unspecialized most, if not all, spccics of grebes, and a diffcrcnce in bill bills arc presumably advantageous. Most temperate-zone grebes shape is also found between the sexes of the Western and move from fi-esh to salt waters for wintering, and this presents Clark's grebes. The first may extend the size range of prey the birds with a different set of potential prey. Some species for ~rielribersof the specics and the second, may increase maj7 make seasonal switches from one kind of prey to another. the ell'iciency in the taking ol'different kinds of prey. For instance, I-Iorned Grebes often breed on small potholes It should go without saying that the nutnber and variety where there are no fish, but are knowil to feed on both fresh- of 11cl11ii1ithparasites found in an individual grebe host de- and salt-water fishes (p. 39). These would be available where pend primarily on the number and variety of intermediate the birds breed on large bodies of water as well as during hosts the grebc consumes, but the establishment of the para- stopovers on migration and on the wintering grounds, sites can be altered by inherent resistance on the part of the respectively. Here, again, new kinds of prey may be available, host or interactions with other parasites in the bird's gut (e.g., and the gelleralized bill form is again presumably an advan- the apparent dorliination of the enteric helminth commu- tage. The importance to parasites on stopovers by birds is nity ol'Rcd-necked Grebes by 1)ioecocc.sku.s asfjeq Stocl<& Holmes illustrated by the case of the nenlatode Bustrongyloides L~~bijex, 1987a). Because differences in bill size may result in differences (p. 29) which relies on stopovers of migrating fish-eating birds in tllc mean size and/or spccics of prey taken, they may affect to complete its life cycle (Measures 1988b, c, d). at least the relative numbers of intcrnicdiate hosts of different After breeding, some species, like the Eared Grebe, make species ol'lieln~inthtaken. This in turn may affect the relative molt migrations to saline bodies of water where they congre- numbers of the different intermediate hosts ingested, but gate and remain during the molt and regrowth of the flight because grebes take a \vide varicty of'thc available prey spccics, Seathers before molliilg on to winter quarters (Storcr &.Jehl the relative nuillhers ofdil'l'erent species of parasites rnay be 1985). This may make hem subject to parasitism by a new cxpcctccl to vary riiore than tlie numbers of species found in range of llclminths whose intermediate hosts inhabit some the birtls. These itlcas nlight be tested by comparisons of food of these waters. habits with parasite loads on spccific bodies of water. Sympatry in grebes and its possible effect on parasites. Whilc Fjeldsii ( 1983a) demonstralcd character displacement The presence of several sympatric species of grebes with var- resulting in rood specializations in sympatric grebes, he also ied diets on the breeding grounds (or elsewhere) presum- pointed out that in isolated areas with a single specics of ably increases the number of potelltial definitive hosts for a grebe, the birds tend to have an "all-purpose" bill "which parasite. This sympatry in the hosts may have been a deter- permits opportl~~iisticfish-eating withor~tloss of the ability rent to the development of host specificity within the grebes. to feed efficiently on tiny arthropods." Yet in spite of One feature of the grebc parasite specialists in general is speci;llizations, all grebes are opportunists and will take al- that far more are found in more than one species of grebc lnost any animal food that is readily allailable. This increases host than in a single one. For example, among the 29 spe- the rangc of inccrmcdiatc host species a grebe may consume cies of the family Amabiliidae, the largest family of grebe ant1 tlius the rangc of helmi~lthparasites it may accluire. Where specialists, 17 are listed in category 3 (grebe specialists, ex- more than onc grebe species occur, this also increases the cept those known only from the type host), seven have been number of potential definitive hosts available to the para- found in two specics of grebes, five in three, and five in six sites. species of grebe hosts. The figures for genera are two in one This general similarity in bill form and the varied diet of grebe genus, eleven in two genera, and four in three genera the grebes contrasts with the greater diversity of bill form of grebes. Of the remaining ainabiliid species, ten are, as far (BPcIard 1969) and more restricted diets found in some of as I can find ol~t,only known from the original description, the auks and their relatives (the family Alcidae). Several spe- the definitive host for one species is unknown, and two are cies ofalcids feed in large n~miberson specific kinds ofswarm- known from a single host, and not very well known at that. ing pelagic prey and thus rnay take few prey specics. These The figures for the 12 nalncd species of Hymenolepididae alcids' prey swarm with their own prey, and presumably are considered grebe specialists (category 3) are similar: three intermediate hosts for cestodes of the genus, illcatamin. The each are known from two, three, and five, and one each from alcids are the definitive hosts and presumably excrete eggs four and six grebe species; and the figures for genera are of the parasite while feeding on the swarming prey. This is three froin one grebe genus, six from two, and two from three, an ideal situation for the development ofboth host specificity and one from four grebe genera. Three other species of in the parasite and specialized bill form in the host. The gen- hymenolepidids are known only from the type host and eral silriilarity of bill form in most grebes, the varied diet of probably only from the original description. While it is by even grebes with bills inoclilied for taking spccific kinds of no means certain that all of the species known only from the 4 (5 M~sc.PuI~I.. Mus. Zoc)~..,UNIV. MICII., No. 188 type host will eventually be known to parasiti~eone or more far larger tll;ln I.akc ,J~~nin,lias a grcatcr varict). of habitats other grebe species, it is likely tlrat sonrc will, and it is also ant1 a largcr fauna of Iislics a~ldinvet-tcbratcs. Having a larger- likely that some will turn out to be synoiryinoLts with better- nunibel- of potential species of intermediate hosts for known spccics. An exception to the general "rule" that nlost helminths, it can be cxpcctctl to have a grcatcr 1lu111bcr01' grebe specialists are linown from more than one grebe host species of these parasites. The fact that all of the grebe spe- appears to be in the l)ioccocesti~~ac,one species of which, cies i~lvolv~drat appreciable nrrmbcrs of insects suggests that 1)iooc.occ~sl~~ts(~coljll~e~, kirowil oilly fi-01x1 ficchj~hcc~)t~c.sdo~ninicus, the helniinths on tllcsc lakcs Ilaviirg these i~ivei-tel~ratesfor is a cornn~onparasite of this grebe in southern Texas, and intcrincdiatc hosts may well be found in all t11~grebe spe- has also bee11 found in that grebc in South Anlcrica and the cies on eitl~erof the lalies. With the possiblc cxccptio~lof' West Illdies. As mentioneti below (p. 54), the differeilcc in the Silvery Grebe on I3aIie.Jrmin,2111 the grebe spccies can bc tlre degree of host specificity bctrvccn the Anrcrican and expected to harbor the same species of parasites using fishes Et~rasianpopulations of L)iorcocv,sl~r.rn.sfivl; suggests that two as interirlediate or paratc~licIlosts. Tlir grebes 011 tliese lakes spccics may be involved. The paucity of cestocle sl>ecics spe- arc residelit, and as indicated by tlrc 1no1-phologic211diffci-- cific to a single grcbe species may bc because restricting the ences between tlie populations of the Silvery and White-tufted number of possible host species would restrict the parasite's grebes on the two lakcs, tlrcrc is no significant movement of reprod~rctivcpotential and therefi~retlre chance of its off- tliesc birds l~ctweenthe lakes. It is not ~~nlikelythat endelnic spring in reaching another host. If this is true, restriction to spccics of parasites might occur on one 01-both of thein. a single grcbe host would need to be balanced or overweighed This is of pal-ticr~larinterest becallsc st~clicndcmis~n has yet by soirlc other Sictor, sr~clras greater egg production, that to be demonstrated for any grebc Irclmintlr. nlight increase the parasite's fitness. Why tlie grcatcr degree The rainbow trolrt (Snl~~rogair(Ln~ri) has bccir i~~troduced of specificity inay be f'o~undin 1)ioc~c.oc.c.sllisthan ill other grebe on both lakes and an atherinid (Odonl(:stht,,t Oonc~ric,nsi.r)(Fjeldsi parasites is unclear, but may be related to tlre facts that the 198 1 a) and tlic lake trout (Snlv~li17rr.r~~n~nc~yc.u.sl~) on Lake species are dioecious, that it is usual for only a single pair of Titicaca (R. I<. Miller pel-s. comm.). The trol~thave cvidc~ltly these large worirls to be fouiltl in one definitive host, and greatly reduced the poprrlations of the nativc killifshes (Orustias that they may produce large nrrmbcrs of eggs. spp.) on Lake Titicaca (K. K. Miller pcrs. coinm.), but it is Although the parasite faunas of the species of grebes on not known if parasites were introduced with thcsc fisl~csor Lakc Junin and the Lake Titicaca basin have not been stud- how the introdtrctions have aft'ectecl tl~cdiets ofthe grebes. ied, Fjeldsi (1981a) lias reported on the diets ofthese grebes. Feather-eating. It has been known for more tlla~ltwo hun- 011 Lalie J~uirin,lie for~ndthat while, on the basis of mass, dred years tlrat grebes swallow largc numbers of their own the diet of the Pu~iaGrebe (Podicc.l,.stnmanoru~ltii), ail endemic feathers, and several hypothcscs have bee11 proposvd to ex- fish specialist, consisted of ail estimated 93-95 pcrcc~ltof fishes, plain this unique habit. Picrsnla rt nl. (1989) have sllmma- only appi-oxinlately 12 percent of the prey itelns were fishes, rized tlre av;lilable iilfornlation on the subject in their strtdy small aquatic invertebrates, especially midges (Chironomidae) of 407 Great Crested Grebes (I'odicc,j).s c.ri.slalus) acciclelltally and watcr boatmen (Corixidae),accounted for tltc rcst. It is dl-owned in gill nets in The Netlicrlantls. After 1)rc.senting clear tliat the clrancc of ingesting a parasite larva from one evidence against other hypotheses, they proposed that the of the last two groups wot~ldbe greater than that from eat- most likely explanation is that "ingcstcd feathers, in the ail- ing a lisli. On the other hand, a fish, which is larger, might seircc of' other indigestible matter; co~itribl~tcsubstance to co~ltaiiia larger number of infective larvae than a srnall ill- the stomach content, enabling the f'or~nationof pellets that vertebrate. In contrast, the related Silvery Grebe (1'. occipi- call be ejected," and that the "habit of'rcgularly ejecting the LNIIs) took 110 fish, while the White-tufted Grebe (liollnnrlicc stoinach contents mininri7es the cllancc that any serious rollnntl) took an even higher proportion of fisll (by mass) population of gastric parasites will build up in the nppcr part than the Puna Grebe but ate rnoi-e large and medimn-sized of the alinlcntary tract." Observations of gl-cbcs dri~lkiilgprior fish th2111 that species. 111 spite of this, it still ate largc num- to pellet casting (r.g., Storer 1961) also suggests that the stoln- 11ei-s of' aquatic invertebrates. Althorlgh two species of fish ach-clcaniirg hypothesis may be the correct one. inhabit Lalie Junin, only one, a cyprinodontid, Orrsliccs, .was Altlro~~ghnot often nlciltioiled or ilifferentiated t'rorn the reported to be taken by grebes. Inass of feathers Gee in the lumen of the stomach, a plug of On Lake Titicaca, the Silvery and White-tlrftcd grebes oc- several feathers is regl~larlyfound lotlgcd in tlie stomach's cur wit11 the large, endemic Short-winged Grcbc (Rollnndirr sinall pyloric lohc fro111 which the upper end of tlie small ,microprercc). Both of tlre first two species differ morphologi- intcstiiie opens. The plug, which is not cast at the same time cally f'roin their counterparts on Lakc .Tunin and the Short- as the pellets from the rcst of the stomach (Wetrnol-e 1924; winged Grebe is far inorc different Go~nits congener than Storer 1969), presumably acts as a filter preventing large the P11na Grebc is from the Silvery. On Lakc Titicaca, the illdigestible objects such as fish bones and rough pieces of Silvery Grebe takes a few fish, whereas the two others have chitin from passing into tlic intestine. In this, it is very effec- predominantly fish diets, the large Short-winged Grebc tak- tive, because inspection of the intestinal contents reveals vil-- ing both a larger proportion of fish 21nd larger ones. Both of ir~allyno large indigestible food remains. This plug has air these I'ish eaters also take a co~lsiderablevariety of inverte- obvious advantage for grebes in prc\,cnting damage to the brates, nrost of them insects. wall of the intestine, and when it is ejected, it may carry lai-- 011 the basis of Fjeldsd's study, I think it worthwhile to spectl- val helmintlls with it. On the other hand, it may have an ad- late on tlre parasite fa~masof' these two lakcs that can be vantage for parasites that reach the ilitestines in rcdt~cingor expected to occtrr in grebes. The Lake Titicaca basin, which eliminating the lilzelihood of their being dislodged. Still, the includes Lake Poopo ancl the river between the two lakes, is plug preselits a barrier thr-ouglr or past \vllich inli-ctive lar- taczanowskii o. juninensis o. occipitalis andinus nigricollis Figut-c 7. An lull-ootctl (1-ccshowing the relationships among the genera and species of'gl-cbcs, based primarily or1 courtship ancl mating I>ehaviol.,patterns or thc downy young, osteology ancl myolo,g of the wing and pectoral girdlr, and plumage. Drawing by John Mcgahan, ~notlilictl1'1-om Fjcltlsi (1!)82;1). \lac of parasites must pass. in conlinon is sucker-like organs on the scolex: two slit-like 111 spite of' this potential barricr, grcbcs ~~suallycontain bothria in the Psc~ldophyllidea,four bothridia that are often very large 1111mbcrsof intestinal parasitcs, especially cestodes. sucker-like in the Tetrabothriidae, and four round suckers I-Iow the larval parasites get fro111 the stomach into the in- (in the Cyclophyllidca). In the last order, an eversible rostellum testine is not known. Those that do not excyst until they reach armed with one or morc circles of hooks is usually present. tlic intestine may well be caught in tlie plug and cast with it. It is possible that before the rostellum becomes permanently Some that excyst before reaching the plug may well have embedded in the lining of the gut, there may be some move- cvolvccl iuethods oP getting past it, but it seems likely that ment of the larva by the altcrnatc attaching and detaching unless large larvae can push past the plug, they may have to of the suckers and the rostellar hooks and extension and wait nntil a time whcn the plug is not in place. Not all infec- retraction of tlie rostellum. If this type of movement is used, tivc larvae of cestotlcs arc small. For example, a single larva I think it far more likely that it would be after the larvae oP tllc grebe specialist, Schistotccenin len,uicirr.us, is large enough reach the gut because the flow of liquids from the stomach (tnean length oP 20 mm) to fill a largc part of the abdomen to the small intestine would carry the larvae with them morc of a full-grown nyn~pllof the large dragonfly, Annx juniu.7 rapidly and without effort on the part of the larvae. The (Boertje 1975).M'heii tlie pyloric plug is replaced is unknown, acanthoccphalans have a retractable, spine-covered probos- Ixrt it might be when digestion is complete. cis. Although how inf'cctivc larvae of' parasites pass this bar- We are left with the likelihood that infective larvae become rier is unknown, it must be at a time (also unknown) when attached temporarily by means of bothria or suckers (in at the plug is not in place. The lack of largc pieces of indigest- least the digenes and cestodes) to the wall of the stomach of ible rnatcrial in the intestines indicates that this must be some the grebe until the pyloric plug is removed, presumably cast time when the stornacll is empty. I think it likcly that these as a small pellet or with a pellet including the larger mass of larvae may attach thcmsclvcs temporarily to the wall of the feathers from the lumen of the stomach. The presence of tligestive tract anterior to the plug, otherwise the loss of lar- attached larvae might be detcrmined by careful examination vae cjcctcd with pellets and/or the plug would be large, and of the stomach walls; finding out when the plug is lost would this would provide ;I str-ong selective advantage for the re- be morc difiicult but could be done by study of captive grebes. tention of rrleaiis of' attachment that could be quickly re- Another aspect to the habit oP feather eating might affect leased. Inl'ective larvae must have attachment organs well the presence of external parasites. Piersma et al. (1989) have developed and these are presumably like those of the adults. shown that grebes show a preference for eating feathers from Tlle digenes found in grebe intestines have two suckers and their own flanks. Because the feathers eaten are not plucked the Echinostomes also have a ring of hooks at the anterior from the bird but come out naturally in the course of preening, end of the body. What the cestodes parasitizing grcbcs have one might expect that there would not be enough flank Slirjabin in the 19201s,a series of All Union Helmintl~ological offers an ~lnusualopportunity to study parasite diversity and Expeditions resulted in such important compilations as those loads under different ecological conditions. The second spe- of' BaruS (11 nl. (1 978) and Iiyzhikov rt al. (1985). Outside the cies, I<. micrqhtri-n, is flightless and is confined to the Lake former Soviet Union the regional coverage has been extremely Titicaca basin. Even with the incomplete data available at variable, being far more extensive in the Northern present, a preliminary co-speciation analysis might lead to a 1-Tcmisphcre, especially in Eurasia, than in the Southern (Table prediction of what parasites might be expected to be found 3).In North America, considerable important work has been in Rollandin if co-speciation has occurred and/or if the fauna done, h~~t,as pointed out earlier (p. 7), funding for has resulted from colonizations (Hoberg 1992). parmiit)Iogical studies often has been roughly proportional Australia, New Zealand, and Madagascar also liave endemic to the importance ofthe parasites (and their hosts) to humans, species of grebes whose parasites need much f~~rtherstudy. and support for the str~dyof general parasitology, never Work in subsaharan Africa, with a grebe fauna of three spe- i~pproacliingthat in the former Soviet Union, has been cies all widely distributed in the Palearctic Region, might ex- declining. Yet the number of hclminth species is great and tend the known ranges of Palearctic parasites, might add para- the nu~nbcrof l~elrnintl~ologistsfew in comparison with those sites endemic to the Ethiopian region to the list of grebe para- of students of sonie other groups, such as birds. sites, and would form a base for understanding the virtually This is partic~~larlyluifortl~natc because knowledge of para- unknown parasite fauna of the Madagascar grebes, wliich are sites can lead to important interdisciplinary stltdies such as apparently the result of a triple invasion of 7i~clzyyBaptu.rfrom I-lobcrg's (1986, 1992) on the coevolution of parasites and the Afi-ican mainland (Voous & Paync 1965). hosts, zoogcograpliy, and evolution of the Alcidae and Bartoli's Few studies of helminth parasites have been made of grcbcs st~~dyof tlic Yellow-legged Gull (Larus cachCn,,nan..srnichalzrlli,~) taken on salt water, where populations of at least eight spc- and its digcnc parasites in (hrsica (1989),which clearly shows cies, including members of the two South American endemic tlii~tthe knowledge of the ecolo 'L~l,lc4. Ntullbcrs of N;lmccl Spccics of Parasites in cach Major Parasite Group Krpol-tcd 11-omcach Grebe Species1. Slxcics Trc~r~. Ccst. Acan. Nelna. I.ecch. Mitcs Lice Total 'Iticludcs those that act as intcrmccliate or paratenic hosts. 21'~~csnm;~l~lyincludcs A. rlrcrltii. Table 5. The Numbel-s of(;l-cbc I-Iclniinth Species in c21cl1I-lost-Spccilicity Category1I)y F'ulrily.' Totnl Sp. ?1 1 2 2 ?:'I 3 ?4 1 5 5 Psilostomidac Cathacmasiiclac Philophtlialmidac Ecllinosro~rlidar (:lino.\(o~iiidac Scliistoson~atidae <;yathocotylitl;rc L)iplostomidac SLI-igeidac O~~istlro~-chil'o~-~~~csOpisthol-chiclac I-Ictei-ol~hyidac Pacl~ytrc~riaticl;~c Pl;rgiorrliifor~irc.a Kcnicolitlae Plagiorchiitlac illicrophallitlac PI-osthogoniniid;~e Ochetoso~natidac E~~cotylidae Digcries Totals (:cstodcs I'scudophyllidca Dipliyllobotliriidac Tctr;~phylliclea 'ktr;rbotllriitlac (:yrlopliyllidc;~ 1)ioccoccstid;rc Anlabiliidae Dilcpiditli~c I-Iy~~~cnolcpididac Ccstodc Totals . ------~~- i\canthoccphalans l'olymorphida l'oly~no~.~~hiclac Ncniarotla Enoplida 1~ioctopliymaticl;re Triclil~ritlae St rongylitla Amidostomatic1;re Ascal-irlida Anisakidac Spit-ul-id;r l~r.acnricrtliclae Tetraniel-idae Acl~ariidac Onchoccrcidac Nc~liatotlcTotals '(;ategories: 1 = (;enel-;rlist. 2 = Specialist in otlicr groups, rarc or occasional in grehcs. 3 = Specialist ill grcl)es, rare or unknown in other groups. 4 = ICriown only 1.1-on1 thc type (gl-ebc) host. 5 = I The sm:rller tl~eprey size, the greater the number of species nigrzcollis, three each Srom Tcrclzybaptu.~rufi'collis and I-'otlicef)s is :lvailal)lc, and, presun~ablythe greater number of parasite auritu.~,two each from I? cristatus and Archmophoru.us occiden.lalis, slxcies ~~otrldbe available in them, and also the larger number and one each from IZollan,dia rollnnd and Podilynzbu.~podicrps. of' indivitluals worrld be needed to sustain a grebe. Stock's (These figures do not include species not known to mature data Gom Alberta (1985) support.. these ideas. The fisli-eat- in grebes.) As a group, acanthocephalans show little specificity it~gW(:stcrn Crcbc (A(,c.hrnoj~horu.soccid~ntrrlis) was host to folrr to host groups, and as yet there is no evidence that any to ten species of' i~ltesti~lal1ic:lminth per bird (mean, 6.4) acanthocephalan is a grebe specialist. All of those reported with a total of' I(? species and a range of 112 to 1,800 parasites fro111 grebes are also known from at least one other order of pcr bit-tl. In contrast, the Eared Grebe (Podicc$s niiqicollis), birds, and most are found in waterfowl, which comrnonly which lbctls priniarily on s~nallaqnatic invertebrates, had two occur on the same bodies of water as grebcs and in most to 15 spccics of Ilclminths per bird (mean, 9.1), a total of 26 specics of these acanthoccphalans, anatids arc the most fre- spccics and frolri231 to 33,169 individuals per bird. The Ked- quently reported hosts. Why so many liave been reported 11eckec1Grebe (I! gri.spgot~cr)had four to 14 species (mean, from F! grisegrnc~is ~~nclearbut is probably diet-related. These 10.7), 21 total or23 spccics and 326 to 10,459 individuals per grebes arc known to take both groups of intermediate hosts I~ircl.The sample of Horned Grebes (1-1 n,urilu.c) was too small as well as fishes that act as paratenic hosts. This reason for l'or a 111caningf111comparison. the greater nlunbcrs of reports of aca~itlloccphala~isfrom f? Althor~~l~as a group, nrore species of cligencs than of any griseg(jn,aappcars to be borne out by Callirnore's data (1964) otlier hellninth group have been found in grebes 5), on Polymorjjhus parodoxus, which show both a higher inf'ec- in the intcstincs of individual birds, tapewornis tend to out- tion rate and greater Incan number of worms per infected tirttribcr tl~enlboth in tcrms ifspecies and individuals (Stock bird in F! grisc~gorr~athan in the other three species he examined. & tIolmcs 198711 p. 670). Means of'2,794 individ~~alsof 'lirlria The fact that eight of the 13 species acanthocephalans known birc,~t~is,1,635 of' l)iorr.l~issp. "P," and 1,183 of 1)ic.rar~oLnrnicr to lnature in grebes are known from one spccies of these /jn,rcrj~ornlrwere reported from 31 individuals of I'odic(:p,s birds (in forrr instances f? gri.sog~na)may similarly be explained ~~igricollis.These three species of ccstodcs are all considered by the infrequency of' occurrence in grebes and the diet of grebe specialists by the i~rrthors,and the numbers attcst to the birds. Diet niay also explain why but one or two species the success of spccif'icity to grcbc hosts in these cestodes. of acanthocephalan have been reported from the two large, Acanthocephalans. Members of one family, five Kenera, and tish specialists, Podicrp-\c.istalu.c and A~clrmophorusoccidentnlis. 13 spccics of this group have been found in gkbes as de- Nematodes. Members of four orders, nine families, 20 finitive hosts in natlrl-c. None is specific to grebcs. Two oth- genera, and 38 species of nematodes are known to parasitize ers, Coiy~io.sorncr,SOIILP~IIU, and C. .strurnos,um, whose definitive grebes. Of these, nine species (22 percent) and no genera Irosts arc tnamm:~ls,pritnarily pinnipeds, are not known to niaturc in grelws or to 11sc them as paratenic hosts, and one, Podilynzbus podiceps Aeckrizoplzorus occidentalis I'olj~~~ro,-/,lrrt,s,/~r~t~~o.s~~~,s,has only been infected experimentally A. clarkii in 21 grel~c.Acantlioccplialans are not comnion in grebes. In their strrdy of intestinal parasitcs of 91 grebes ofli~rrrspecies in Alberta, Stock & Ilolnics (198711) reported a maximrnn of' 12 pet-writ of the individuals of any species (P~dic.~fj,sgrisrgrnn) Taclzybaptus dorninicus ii~fectedby a spccics of' acanthocephalan (C:oryr~osorna ~OII.SI~~~.~III~I)ant1 the highest incan n~~mbcrof' individuals per 11arasitizcd birtl was ten (immature) Polymorf,/rrr.sI~~LI-ilis in I'odic/.l,.s nigric.olli.s. Gallitnore (1964) reported a higher rate ol' inkction by 1-1 [~c~rncloxrc.~in smallcr sarnplcs and a maxi- i? r[rficollis I? rzigricollis mlnn ol' 11 2 intlividuals of this parasite in a single grebe. According to Holmes (ill lilt.), Callirnore's sarnples iilclr~dcd I? cristatus 11ra11yi~nn~:lt~~re itldi~id~~als, incl~~ding examples of I? mcrrilis. I? (;allin~orc sampled a widcr variety of l~abitatsthan Stock, auritlrs ,~ntlit is not ~unl~kelytlint in sonic the grebes fed to a largcr I? grisegena cxtcnt ot~gammarids, wllicli arc tl~eintermediatc hosts of F! Rolltmdicr r-ulltrrzd ~~ccrrili.~. Thc intcrmetliatc I~ostsfor nine of tl~c13 species known to nlaturc in grcl~csarc known. All are crustaceans, either ~rmphipodsordccapods or both. The number of species of intc:rmcdi;rtc hosts appcars to be tlirectly related to thc ~~u~nber to ofst~ttlicsol'tlic lil'c cycles. The sarrle applics- - the paratenic hosts. In one of the best-st~rdic:dspccics, Corynosomcc .str~~rnosrrm, :39 sprcic-s of fislics of 19 la~niliesp111s onc snake have been TACHYBAPTUS ROLLANDIA PODICEPS 1.cportu1it1 this category, and jl~venileI'orms liave also been LINE LINE LINE I'ortnd in men~bcrsof three families of carnivorous mam~nals, 1111t arc known otlly to mature in pinnipeds. Figure 9. Tht-cc lines of grebes for cornpat-ison with the groups of' Aylcn71irrnus(Table 7).The species in bold face arc those hat-boring Acat~tl~occpl~ala~~shave been reportetl Prom eight species the species of A~zcnnirrn7r~discnsscd by Edwards (1965). ol' grcl)cs: tiine species horn Por1icr.fi.sgris~genn, four from 1-1 x~l,lc (i.Tl~c. I)is~~-il)utio~~ of Mite Spccies o11 GI-chcs. -~ -- ~~ ~~ ~ -- 7pac .I lyl~aptusLi~rc. Pocliccps 1,inc .. r~~~~ '1; 1io71(1(,. 7: r-ujfc.. 7: (LUIII.1'. ~O(/I/.1'. (II(I: I! XI-LS.1'. (I,;,\/. I! IIIX~I.At. sp. l)~~l~lll(lll,y.\.\o;(/(,/l Rhi~~o~iyssitl;~c Rhy II~II~\.~II\nlh~,r-lr + H/~)~~iorri.\sri,c.ol?~mbit ol(i /?/~~IIO~II,\.\ 11.7 /IO(/I~.I/)P(/IA R/I~II(III~\.\11, ~lOd;/~lll/~~ ~?/I~I~(II~IT.\~~.\/~nl~or~~/~l~n/~ + + /'/I/OXPII[IS ~.oL~wI~I t l'tilox(,nli.\ r~icljo~ + + + + P/i/Ox(,li 11.7 Sp. 1. Schii~ir-0lic.hi6.s rl(,gcr~i.\ + + rl ~lnlgoitlcti La~~ri~~osioptici~~cI'otl~~i/~~tlrt o~JL(J.\ (IIIIPI-~((~I~ I(\ + Xol;~lgidac I17gr-ns.\icr c.o/y~n/)i t i-I ~ ~ ------'t\ccorcling to C:;~ucl (19'74), the ~nitcsfrom 1'. rrig1-1col11~in h4o1-occoa~-c vcry close to I. (oly1ri/17,if not idcntic;ll tvith it. ;Ire considerccl grebe specialists. Thrcc of the nine spccics Helminths. To date, there has bee11 oi~lyone attempt to ofspccialists are known only frorn the original tlrscriptions, relate co-speciation of g~.ebcswit11 theil- hclminth parasites. and two of'thesr are placetl in genera with other species known Stock (1985) cornpa~.ctla pllylogeny ofthc grcbcs wit11 those to parasitize gl.cbcs. Tllc six otlrcr spccics of grcbc specialists of truo genera of amabiliid crstocles, Schi.s/o/opninand Tlic/ri(i. are known from thre? to six species and two or for~rgenera MThile his phylogeny of modern grel~esis in general agree- of grebcs. T11~l-vis no strong rvidence that any spccies of ment with that of I;jrlds:~ (1982a) and Figr~re7, these nciiiatode is a specialist on a single species of grebe. phylogenics ;Ire not cladog~->~msand inclr~tleno rnoleclila~. The species of nematode grebe specialists belong to thrcc information with \vllich to compare thcnr. Stock took the fossil 01' the I'or~rortlcrs and Gve 01' the eight families fo~~ndin rccol-d of grebes back into the Crc~accouson the basis of g~.ebc!s(Tal~le 5). Why is it that while 1n;11iy i~~t~stin;~lheln~inths arc grebe Rich (1983, Fig. 9-17), who shows five 1111spc.cified genera of (:rctaceoi~sbirds as possibly helonging to the grebe line. It specialists, few, if any, will pl-ovc to sl~cciali~cOII a siriglc spc- cies ol'grebe? In general, grcbcs spc~ltlrhc brcctling sc:ason is now helic\~ed(Fcdrrccia 1996) that thcsc Cretaccorrs div- on eutrophic bodies ol'water with a wide variety of potcntial ing birds rrs~~ltedfrom a m~icliearlier radiation than tli;lt prey sp~cies,and as pointed or~tearlier (Results p. 43), al- ~llicliprodt~ccd tllc gl.cbcs. On the Imsis ofa presunied ear- tho~rglia grcbc may takc ;I large Inass ol'tlie p~-cyon wl~ichit lier (:I-etaccous 01-igin for the gi-cbcs, Stock based his specializes, it usually taltes sm;~llermasses of a considcrablc 7oogcog1-aphyof the g~~bcson the breakup of'C;ondwa~ialarrd, variety of' otlicl. kinds of prey. Furtl~ernlore,it is coliiinon which probably took placc too early to account for the tlis- I'or two or more spccics to nest oil tlie same body of water, tribl~tionof Recent grebes. hence, it might well bv disadvantagcor~sfor a parasitc to be Isolated tal-sometat:u-si of diving birds al-c often Sound as restricted to one species of' grebe as its definitive host be- fossils, anti it should be notetl that there is much convcl-- cause that wor~ldredr~ce the nrimbcr of potential hosts avail- gence, as well as divergence, in this ?lement of diving birds. ;~bleto it ant1 thus reduce the potential n~~rnbei-of of'f:sp~-ing This makes itlentil-ilig these bones to 01-tlcrdif'ficult witll- it might protl~~cc.(A similar situatioil presumably obtains out illaterial of otlivr parts ol'the skeleton. The earliest fos- on the Inany wintcriiig gror~~idswhere more than one spe- sil krlowii ccrtairily to Iiave I~ccria grcbc, is of Oligocene age cies ol'gl-ebe occ111-.)This inay have or have liad a darnping (Nessov 1992),and becar~scthis fossil is very sin1ila1-to Recent effect on the cvolr~tio~lol'spccilicity of lielrni~ltlisfol- single grebes, the grebe line probal)ly diverged f'ro~iiot11e1- lines of specics of grcbcs. motlrrn water birtls much carlier. Some members of the genlls I)io(~c.oc.c,.s/~r.smay bc exceptions Thcrc is co11sitlc1-al~lctlcl)ate on whcn the iiiqjor mtliatioil 01' to the gener;~l1-1ile that kw or no species of cestotlcs arc rriodern birtls took placc. Cooper Sc Pen~ly(1997) present a co~n- slwcilic to single specics of'grebes. Why this should be true I~inationol'n~olecul;~~- and fossil rvitle~~ces~gg~sting that there is a question that might he worth investigating. was a (:retaccoris divcrsification of birtls and ~nannnalsrathcr POSSIBLE COEVOI.UTI0N OF GliEHES than an explosive I-adiation of' thein in the E211-lyTcrtial-y, hut AN11 TI-lEIR PARASITES while there is fossil cvidencc for this in scvc~.alothc~. groups, Cooper Sc l'enny cite none Sol- the grebes. On the othcr hand, For srrmmi~~.icsof ~hcnrcthotls r~sctlin rnaliing studies of ~~d~~~i~l,vlicves tlli,t tllere I.atliatiOllsof birtls in tile host-parasite co-speciation anti their importance in various (;retaceorls,Ileither ofwllicll illclrlded birds of nrodc,.n 111-anchesof biology, see Hobcrg 6.1 (11. 1997. and that the orders of Recent birds arose in the five nill lion or so years ii~llowingthc major extinctions at the Cretaceous-Terti- the co~n~nuniticshave been those of intermediate hosts, a1.y ho~u~tla~y.Tliercl'orc, in the lacli of'good fossil evidence, the odonate nynlphs to a corixid bt~gin the case of Trcl7-ia biremis time ol'ol.igin of the grebes is moot. and to a mayfly ny~npl~in that of 7: hiuncin,aia. This sllggests MThilc a co-speciation analysis might provide speculation a parallel with two species of Schisloc~phalus,each of which is ;11,o11t the parasite l'aunas of the grcbc genera (liollnndicc, specific to a different genus of sticklebacks (Casterosteidac) I'olioc,c.j,h(rlrr,s and PodicP/)hor?ts) Srorn which arnabiliid para- as an intcr~ncdiatehost yet is found in a great variety of sites arc 1101 known, I bclievc that far better compariso~lsof definitive liosts. thc pliylogcnies of grebes and ilicse parasites could be made Molecnlar studies on both the grebes and their Iielniinth with saml>lesfrom these genera, the first of which is believed parasites would be particularly valuable for comparisons with nearest to thc arrccstl.al stock of the grcbcs and the last two the n~orpliologicaldata in co-speciation studies. a1.e ol' ~~nccrt>linposition with respect to the two principal The other family of cestodes known to contain several spe- li~ics1.csrr1ting in the genera 7irc./z~l/~crf,tu.sand I'odilym/)lts on cies that are grebe specialists is the Hymenolepididae. the one 1ia11dand I'otlic.c.l,.s a~ldA~c.hmof~hor,crs on the other. In Although Vasileva c.1 (11. have made considerable progress in addition, I an1 by no mealls convinced that Stock's associa- sorting 0111 the relationships of the Palearctic spccies, more tion of grebe species with parasite species in a cocvolutionary work with those fi-om other regions waits to be done, hence scnsc is entirely correct. Similarly detailed data Srom other it is not yet a likely one in which to evaluate co-speciation. con~~nunitiesthan thosc hc stcrtliecl are lacking. It is entirely The digene family Ecllinostomidae is another family contain- ~~ossil~lcthat what may be the principal host in one area may ing numerous grcbc specialists, but it is also in need of a not I,c in another. Folrr- of the an~abiliitlspecies appear to careful rcvisio~ibefore co-speciation with grcbes can be 11~known only 1'1.om tlie original tlcscl.iption (three from attemptrd. I see no other helmintli family as a likely one Sol- 7irc.lr~~l/)cr/~/1r,srr!/i'c.olli.s, and one li-om PodilymOus porlic.r$.s, both such studies. comnron, ~vitlcsprcatl,and easily collected spccies),so assign- External parasites. Because tlie mites and lice parasitizing ing a corc spccics for these is I)y no me;uns certain. The de- grebes spend all their lives on their hosts, they night be likely finitivc host 01' one spccics (7'nlricc,frihrmcrn17,i) is unknown, to speciatc more rapidly with their liosts than grcbes' so its corc species as yet cannot bc determined. Forrr species Iielmi~iths.If this has orc11r1-ed,it should become apparent 01' '/i~/ri(rliavc Ixcn dcscribcd since Stock completcd his dis- through comparison of the phylogenies of the parasite and sertation (1985), and tlescriptions of several of the earlier host groups. For making preliminary comparisons, I have spu.ics lacltecl sl~l'l'icicntlnorphological data to be included divided the species of grcbes into three groups or lines (Fig- in his analysis. Tl~creSore,there will be 2111 excellent oppor- ure 9): a basal Rollnndin line and the T~~chybnf~~1,lu.c-l'oc1ilyn~bu.s tu~~ityto make a more co~riplctcanalysis when rnorc basic line anti the Potiic~f~.s-Aeclz,~nophorusline which form major information is available. Bcca~rscof the community-based na- br-anclrcs of the similar phylogenies oS grebes by T;jeldsd (1977, ture of'thc analysis, informatio~~o~i intermediate hosts lnllst 1985) and Storer ( 1967a and Figure 7). I'oliocr~~~knlu.~and also Ile i~~clr~tlcd.I'el-l~aps thc most significant crossovers in I'odic.eplr~oru,s,whose relationships to the others are less well T~l~lc7. Dis~riblltion and Hosts oS1,icc of the Gc~iusAylrni~irmus Aqrrcrt~ir~r~u.\spcai.ics GI-chrhost C:~.cbeGroup Hrniisphcre 11. nrtslrc~lis Poliocc,f)hali~sriifi)pcc.f ras ? E A. bcrl~li 11. ~/l/~lli/~~i~~lll7 it. cr~ni,~/c.c/i~rrs 11. Or~rc~tri/i.s/i~ cstablisliecl, are omitted. Two specics of the lousc suborder Amblyccra are kno~ln C:oots (Puliccr) arc common in hahitats where most specics fro111 grebes. The first, I',s~~c~do11e(~noj)o17cloliu,~tr, is confinecl to of grebes nest, and this association lias probably been a long grcbes, ~vithone questionable record from a loon. It belongs one. Ass~r~ningthat the region with the greatest nl~mbersof to a genus of 17 species ofwhicli 12 of' tlie remaining 16 are spccics of a gro11p is likely to be the place of origin of the found on rallicls incllrding one, I-'. piloscrm, cvhicli has been group, the coots, lilte the grebes, probably arose in Sol~th foluid on six species ofcoots, two on other gruiform birds, America, where six spccies occur (Blake 1977),while no more and two on charadriiform bircls (PI-ice1974). The similarity t11;ni two species of coots are fol~ndon any otliel- contine~lt 01'1'1 pilosunz to 1-1 rlolizim (Price op. cit.), the fact that these (Peters 1934). Beca~~se,as me~itioned bcf'orc, coots arc conl- two specics are the only known intermediate hosts of t11c nclna- 1no11thr~~~gliol~t nluch of the ranges and habitats of grebes, code, I'i~l(~ei~c~sfi~lic.n~a/rn~,wllicli has been fi)111idon both coots have aggressive interactions involving physical contact with ant1 grebes, and the rclativcly ti-cq~icntcontact ofgrel)es with grebes, get up onto, and even take over; gl-ebe nests or mating coots strongly suggest that grebes obtained the ancestor of' platforms, and mixed cllrtches of coot and grebe eggs have P. idoliunr, and hence /'c~l(~c.i/u.sJirlic.n~c~trrr~,from these birds. bcen found, they are the most likely birds with which grrbes This s~rpportsClay's idea (1957) that Ps~clclon~~nopo~e"has can exchange ectoparasites. The Pact that coots and grel~cs possibly beconie secondarily established on certain water and bclo~igto two different, unrelated ordcrs of bircls is strong 1nars11birds." The second spccics, I,cro~r~,obot/zrion,\inzilP, to whicli evidence that the sharing of groups of external parasites is Price (in lit/.) believes all reports of this genus fi-o~ngrebes not the res111t ofcom~nonancestry b11t of crossing ovcr frorn belong, is very similar to L. cctrunr, which was describccl fi-orn one host to a~iotller. a coot. Most (24) other membel-s of this large genus are found All of the 12 species of mites found on grebcs arc known on falconiformcs, with lesser numbers of spccies (five, in- only from these birds. Five species of the rllino~~yssidnasal clucli~lgthe orie on coots) 011 gruifi)rmes, ant1 members of mite genus Rhi,nonyss,iishave bcen reported from grcbcs. Tllc several other groups I-Iopkins 8r Clay (1952). These authors reported degrees of' host specificity of a single species of these believed that the species of Lnc~n~oBotle,rionnot found on niitcs range from l'otrr spccies and two genera of' grebes to Palconiform birds might be consiclered to belong to a sepa- one species of mite to a single species of grebe and of geo- rate subgenus. Beca~lsrmore species of both l'soudonionopo~e graphic ranges from Eurasia, Australia, anel North America arid Lcc~rnobothrio17are founcl on rallids (including coots) than to a single continent. From this, there appears to be no pat- on grebes, I think it more likely tliat in both instances crosso- tern of'spccificity. Tllc st~ggestionby Pence (1972) tliat each vers occurred [I-o~ncoots to gl-ebes than uico v~~:scr.It is also spccics of' Rhi~n~oriy,s,su,sI'olrnd on grebes will prove to l)e spe- liltely that the crossover from coots occ~rrrcdfairly recently cific to a single species of grebe remains to be demonstrated. t~ccalrsetlrc single spccies caclr of I',\~udo~~z~no/~onand Tlic single spccies of the ereynetid nasal mite of the genlls I,a/~mobo/hrio~cknown from grebes parasitizes several spccies Nc~oOoyn'ninreported f~mmgrebes shows no specificity to a single of grcbcs without significant reported dilkl-elltiation. grcbe specics, 1lavi11gbeen reported from threc species all In contrast, tlic only genus of the lousc srrborder 1sch1locc1-a in dil'l'crciit gcncra and in two of' the tl~reelines of grebes. (Agumni~tn,us)known with certainty from grebes has been Ihund Tlircc spccics of tllc f'catlier nlitc gcn11s Pti1oxmu.s are know11 only Srom tllcsc birds. Accortli~igto (:lay (1957), this genus f'rom grebes. Each is confinc-d to a single genus of grcbc, hi^ no obvior~srclationsl~ip to ally otller and tl~rowsno light with a ~iiaxim~~mof four species in the case of I'lilox(,nlrs Inn- oli the relationship of' its Ilosts." With the exception of thc jor on the gent~sPo/lic~ps. While this suggests a possible rnitc genus, Rhino~7y,s,su,s,this is the only genus of'ectoparasites cxa~ilplcof coevolt~tion,i~lfor~ilation hom this group of ~nit~s which appears to liave spcciatcd 011 grcbes. Aguc~iri~-~n~u,shas 1.1-om the f'o11r rrmaining genera of grebcs, cspccially Rollcrndicr, the most dcscribctl lb~-ms(1 1 species, o~~cof which was cle- ~vot~ldbe important in providing corroborati\/e e\~idence. scribed as a subspecies) of any genus of ectoparasites known Fcatlicr mites ol'tlirec other genera are known f'rom grebes: from grebes and has been divicled into threc specics groups Schizerro1ichu.r rl(:$.nn,.sis reported from two specics and gcn- by Edwards (lY(i5).This degree of tlifferentiation indicates era of the 7iic/eyl)(z/)/t~~line in tlie New M'orld, tlie non no typic that it lias probably been on grcbcs fill. a lo~igtime a~ld,there- genus I'odicipc~dicoplc.~is only ltno~vnfrom Podilymbus fiotlic(;(,.s fore, is the most suitable group of external parasites for com- in North America, and tllc genus I77grc~ssiais reported f'rom paring its phylogeny with tliat of tlre grcbcs. two species ofgrebc in two gcncra in different lines, in North With one exception, each of these forms of Aq~rctniri~~~r.ris Africa. All these three genera of f'eatlier mites belong to known frorn a single grcbc spccies. Tlle exception is A. dil'fercnt hmilics, anel the hct that all have been reported ro1y1nhin1r.sreported from both I'odico~~.~nurit,u~ and I? nigl-icollis. horn the 'lircl~yh(~f)tu.sline of grebes and only one from anothcr Howcvcr, in llis revision of' the genus, Edwartls (196.5) sug- line (Table (5) may be a matter of sampli~lgbecause tlic spc- gests that spccirric~lsfi.o~ii the latter grebe may represent a cics on which these mites liave been f'oc~ndarc both widespread diffcrc~ltspccics. and easily collectecl. Edwards' division of' the f'orlns of Aqucr?zin-ncus into three Mitcs of tlie gcncra Rhi~no,rej~,ss~~tsand NooOo~~claicc Iiavc been groups was based on unspecified "morphological gro~rnds" reported from coots (I'e~1ic.c~)by Pence (1972, 1975), which (op. cit., p. 932). They are shown on his table (p. 933) with suggests a possible source ol'niites of tliese genera on grebes. their grebe hosts and the hrrnisphcres from which tlic spe- Members of tlic sttbf'arnilp Ingrassiinac arc folnltl on birds cies of' lice are known. Edwards' classif'ication of the grebes of I6 ordcrs including the Gr~~if'ornles(Gaud & Atyeo 1996), is o11t of date, and his figure contains sc\~cralerrors, wliich I so coots might well be a sourcc of tliese mites on grebes (or have corl-ected on Table 7, and to which I liave added the wic/~~t/~r,s/e) . gror~psto\vIiicll the grebe specics belong. I have also bro~~glit thc grcbe classification wliicll Edwards 11scd l~pto date and added the species Aqzic~nirmri.~ciu.stralis described by Kettle Reproductive isolation between species of lice has not been (1974).Assu~ning that the pl~ylogeneticrelationships among studied, and subspecies in that group appear to be defined both groltps arc correct, one might expect a large degree oS purely on the basis of slight differences in morphology. The congruence between the relationships of the grebes and those finding of subspecies of the same species of louse on the of the parasites if co-speciation llad occurred. As Edwards Old World Little Grebe (Tacl~ybaptusruficollis) and the New has pointed out, this is clearly not the case. The relation- World Least Grebe (7: dominicus) is odd, because these spe- ships appear to be geographic rather than phylogenetic. cies differ considerably in morphology and may belong to The hosts of each of the three groups of Aquan,ir.rrrusin- different subgenera, or accordiilg to some (e.g;. Oberholser clude at least one lllernbcr of the 'Ihcl~ybril)tu,sand Podice/).s 1974, K.E.L. Sirninons in lilt.), even different genera. In lines. (No species of Aq~unizi~tnushas yet been reported from Edwards' figure, they are placed in the same species! If their liolln~tcliii.)On the other hand, as Far as known, members of Apanirmus parasites are as similar as Edwards indicates, there the e*tre,:sonigroup are confined to grebes in the New World, presumably was a transoceanic spread of one to the other. except that A. rmrr,son,iis found on the E-uropean race of I? At present, the shortest distance between the ranges of the grisc~g~rtcr(as well as on the New World race of the same host two grebe species is between South America and Africa. species); the bahk group is confined to the New World ex- Another possibility is that contact across the Bering Land cept f'or the Indian-African race of 7: ,rulj'coll%s,and the A. Bridge rnay have been made during a warm interglacial period. colyrn,hinrisgroup is confi~rcdto the Old MTorld. No species of Aquanirnzus has yet been described from the If the reports of both I'o(lic.c;l,.r ccuril,u.sand 1'. nigricollis ap- six species of grebes cndcmic to Sour11 America and but one ply to the same species of the c.olym6inris group, the crosso- of the three endemic to the Australian region. Mallophaga vcr fro111 one of' these llosts to the other was presumably a from the South American grebes would be especially valu- recent one. A likcly rncchanism f'or such a crossover is incli- able in comparing relationsliips between the parasites and catecl by the report oPa mixed pair of these two species back- their hosts because the greatest diversity of grebes (five genera brooding and feeding the same chick (Dennis "et nl. " 1973). and nine species) is found on that continent. Furthermore, Ilhcl~y0c~~)lu.srz~ficollis, I'odic.rp.s auritus, and I-'. ni~ricollisall the endemic genus, Iiollandia, is intermediate between the 11avc l~lallophagaof both the bahli and co1ynzbinu.r groups. In two lines of grebes and may be considered nearest the ancestral the case of the first, the European race hosts a n~enibei-of form oS the family. the co!y~~t~bi7zu.sgroup and the Indian-African race one of the The genera to which the other five species of lice found bcihli group, whereas in the other two grebes, the split between on grebes belong, Pseudomenopon, I,aemobothrion, and Incidifrons, parasitc groups is bctwccn the New and Old Worlds. (the last listed by Malcomson [1960] from Podice/)s n,igricollis) This lack of congruence between the phylogenies of the all are known from coots (Fulica), as are two of the genera oP grebes and Aqutr~zirm,ussuggests either that the parasite be- mites (lihiii~on~ss,usand N~oboyrlaia)found in grebes (p. 60). came established on grebes rather late in their radiation, or In summary, there is as yet little evidence of congruence that crossing over between species of grebes occurred rather in the phylogenies grebes and their external parasites. The frcq~rently,or both. three species oS the mite genus Pliloxenus known from grebes Clay (1957) pointed out that there is a tendency for sonle are each known only from a single genus of grebe and each lice to be larger on larger hosts. The species of grebes vary of species of the genus Rhinonyssus may turn out to be con- qreatly in size, t11c s~nallestweighs ca. 100 g and has a wing fined to a single species of grebe. On the other hand, the length oPca. 100 mrn, whereas the largest weighs ca. 1600 g. evoll~tionin the louse genus Aquanirmus is better explained and has a wing length oS ca 200 mrn. To test whether size oS on geographic than on phylogenetic terms. What does seem parasite is related to size of host, I compared Edwards' (1965) apparent is that coots arc the most likcly source of several of measurements of head length and width of the species of the ectoparasitic genera infecting grebes. Ag"~(inirtnu,switl~sizc of the host. The results were inconclu- Again, it is clear that Inore collecting, especially in South sive. The three largest grebes known to be parasitized by America and Australia, is needed. When this is done and when Aq~iani~mus,Podicc.j,s griscgrrra, I? c.ristatus, and A. occidrn,talis, we know more about where on the birds' bodies the lice oc- all are hosts oflarge spccics of Aqunnimzus, but so is the sn~allcst cur, further research on the evolutionary relationships be- grebe ( 7iicl~ybriptusdominicu.~) . At this stage in our knowledge, tween these external parasites and their grebe hosts should such a comparison inay be f~ttilebecause we do not know yield interesting results. what parts of the bodies of the hosts these lice inhabit, and Future coevolutionary studies. Studies comparable to that the variation in sizc and texture of feathers on a single grebe of Hoberg (1986, 1997; Hoberg et al. 1997) on Alcataenia is considerable. and its alcid hosts have not been made on grebes and their The cxccptiolls to the rule that each of the groups of parasites. At present, opportunities for this seem limited. In Ag"(ini+n~,zisis confined to one hemisphere pose interesting the case of helminths that are grebe specialists, most species questions, but I doubt that we have enough information or that are well studied are known to parasitize more than one specimens to speculate on their origins. The description of species and often, more than one genus of grebes. As pointed A. h. chntr~h(!rliniis based on only three females so the inale out earlier, this is probably related to grebes' breeding on geniialic characters arc unknown, and Edwards' suggestion eutrophic bodies of water in which a wide variety of poten- that both Podict$.s nrrr.iL,usand I? nigricollis arc host to the same tial prey (and thus of infective stages of parasites) occur and species of Aq,ua17,irnzusin the Old World is weakened by his the grebes' habit of taking almost any kind of prey that they comment that the parasite populations on these two species they encounter (p. 45). Tlil~s,they acquire a wide variety of "may 11ot bc conspccific." parasites. As a group, grebes tend to forage near their nests duce tlle amount of hypersaline water taken in with the food on Mono Lake. However, the alkalinity would presumably and llcilcc t11c amount of cilergy needed to excrete the ex- be neutralized by sto~nachacid so that by the time the stoin- cess salt. These lakes may also have the ad~lai~tageof con- ach contents reached the intestine, the pH presumably might taining large supplies of hod to which access is limited to be nearly similar in birds on both sea water and fresh water. tlic few specics of birds that can tolerate the conccntratio~l The presence of other ions in the water might also cause the of salt. helminths to be killed or to leave. In any case, it is probable Grel~es,especially Eared Grebes, carry ~musuallylarge num- that high levels of dissolved salt and other minerals, pH, or I~crsofllclmiiith parasitcs in the small intestine. In his study a combination of these, would be responsible for ridding ol'fotrr grebe species in Alberta, Canada, Stocli (1964) found the birds of intestinal parasitcs shortly after their arrival on a range of'froln 231 to 33,169 such parasites in the 31 Eared the lake. Grebes he examincd. He did not give a figure for the mean How might the loss of parasitcs be important to the birds? ilumbcr of hclmiiiths per bird, so I calculated a rough esti- Most of the co~nmoillyfound parasites in these birds are small. inate of this by su~n~ningthe mean number per bird of each Tutrin hire7nis range from 1.5 to 3.3 and T decacantha from of the 26 species of parasite fo~lndand dividing this by the 1.0 to 7.0 mm in length, and the fluke, Pctasiger nitidus, is in n~umberof birds examincd. The resulting figure was 7,407, the same size range. Other cestodes like Diorchis and several more than twice that for the Red-necked Grebe (3,116 for other hymenolepidids, arc long but narrow, with widths of 23 spcciesof lielrnintlis). Figures for the Horned and West- roughly 1 to 2 mm. This means that the surface area of the ern grebes were even smallcr. enormous numbers of these small a~lirnalsmust be very large 1,arge numbers of small invertebratcs makc up the bulk in proportion to their mass and must have tlie capacity to ofthe Eared Grebes' diet. This includes intcr~nediatehosts absorb large a~no~~~itsof nutrients. In addition, the damage ol'lnany I~elininths.Tlllls, t11c birds are sl~bjjectto higher in- caused by the implanting of thousands of attachment organs lkction rates and larger numbers ofi~ldividualsof these para- in the lining of the intcstine must decreasc the birds' ability sites than grcbes that fccd on smaller numbers of larger prey. to absorb nutrients. This decreased absorption of nutrients Jelil (1988) found few or no intestilia1 parasites ill the many by the birds must be addcd to the energetic cost of remov- Eared Grebes taken on Mono Lake, where the salinity is ap- ing excess salt froin the digestive tract through the salt glands, proximately 2.5 times that of sea water and the water is also and the energetic needs for the dcvclopment of new feath- highly alkaline (Mahoncy ScJehl 1985).The cestode, Confluaria ers. /)odici/)in,cr, which is a core species of helminth in Eared Grebes The invertebrate faunas of saline lakes are few in species, I'rom fresh-water lalies in Alberta (as "L)ub%nin~olepispodicipinu," but brine shrimp (Arternin) are cornmon in many such lakes, Stock Sc I-Iolmes 198711) is k~low~ito have a life cycle with includi~lgMono Lake, where they arc abundant and form Artpmia and these grebes on Tengiz Lake, a saliilc lake in the principal food of Eared Grebes. The fleshy tongue and, ICazalihstan (Maximova 1981). The virtual lack of ccstodes presumably, the habit of pressing food against the roof of in grcbcs on Mono Lakc suggests that Mono Lake is too saline the mouth are shared by the Eared Grebe's South American to sllpport a cycle of C. porlicit,in,n (or any intestinal helminth) relative, the Silvery Grebe (Podiceps occipitalis) , which Wetmore citlicr in Arternicr, which is the principal food source for the (1926) found in Lake Epiquen, Argentina, a saline lake in grebes 011 tlic lalie, or in the grebes. Assuming that parasite which Artemia were abundant. Tlie time was December and species vary in ranges of tolerance for or have diffcre~it the grebcs were courting, so they were presumably not molting, prefcrcnccs regarding salinity, this, in turn, might well account but it is likely that after breeding, they would return there for theil- dying or lcaviilg the host in response to a change in on a molt migration or for both molting and wintering. the salt concentration in the intestines when the birds move Mono Lake may be unique or atypical in its extreme salin- from fiesh to salt water, and vicc ucr.ru. ity and alkalinity, the superabundance of food, and the pre- Jclil (1997) showed that prior to their migratory flight from sumed lack of intective hosts for parasites. Although I have Mono Lake to their wintering grounds on the Salton Sea or bee11 unable to find data on the salinity or alkalinity of Tengiz thc Gulf of Calii'oriiia, Eared Grebes decreasc the mass of Lake, in Kazakhstan where a population of the cestode their digestive organs, which in turn dccreases their wing (Conluariafiodicifiinu) is able to survive (p. 24), it presumably loading. This is especially important for birds like grebcs has a coiisiderably lower salinity and alkalinity than Mono for which this figure is extremely high. The loss of several Lake. Comparisons between situations regarding salinity, food thousand parasitcs, even though small, would decrease the abundance, and presence of intermediate hosts for grebe wing loading even more. parasites on other saline lakes to which Eared Grebes move On Mono I.akc, the salt content oiwater entering the stom- might shed some light on why the grebes move to these lakes ach (and tlie intcstine) would be even greater than when and also might offer clues to how this habit may have evolved. the birds are on sea water. This greater salinity might result The ecology of intestinal helminths in grebes. In their broad in the birds' losing the parasites faster than on marine envi- study of the determinants of comm~lnityrichness in the ma- ronments. Although Eared Grebes greatly reduce the intake jor groups of vertebrates, Bush el ul. (1990) found that aquatic of water with the food by pressing food items against the birds tend to have more parasites than any other major group roof of the mouth with their fleshy tongue (Mahoney & Jehl and describe them as "the 'tropics' of the parasite world." 1985), an appreciable amount must be taken in, because a This is particularly true of those found of fresh water, and of considerable amount ofwater must be held among the many these, grebes may well prove to have the most. Bush et al. apl~iidagesof these crustaceans. also introduce the term "component species" for parasites Allialillity irlight also be a problem for hellninths in grebes which are found in ten or more percent of the hosts in a study, a tcrir~which is vall~ablcin eliniinatil~gf'~-orn coinpara- pal-asitc fa:,lr~nas.This is supported by the Sact that of' the 51 tive studies spccies of' only incidental oi- accidental occur- named specics of' cestodes and acanthocephalans reported rence. from the Ked-necked Grebc, only 15 (plus two species not Stock (1985) determined the size and distribution of in- identified wit11 nanled species) were fountl by Stock, and the tcstinal hclnlinth faunas of four species of grebes on the breed- comparable figures for the Eared Grebe were 40, 20, and ing grounds in Alberta, Canada, by quick freezing, tying of'f' seven. The data for the Horned Grebe are too small for the length of the sinall ii~testineinto twenty equal sections, meaningful colnparison. All three of these species of' Podice/)s and counting the n~unbei-of each lleliniiltll species in each are widely distributed in Eurasia where they arc sympatric section. This resulted in 1nucl1new inf'ormation on tlrc abun- wit11 the large, fish-eating Great Crested Grebe (P crislalus). dance and distribution of' these parasitcs within grebes. In I11 areas where this species occurs with tlle lied-necked Grebe, the 91 indi\~id~~alsof f'ot~i- species of grebes that Stock exam- the latter is smaller and shorter billed than in North America ined, he found each bird infected by from two to 15 specics and, at least before the rapid recent noutllward expansion of 11elminths. This is a greater percentage than those reported of the range of the Great Crested Grebe in Eurasia north of fro111 else\vhere by Rausch (1983) but is consistent with the breeding range of the Great Crested. This difference was Rausch's statenlent that "hig11 rates of infection arc typical reilectcd in the higher proportion of fish in the diet of the of birds that feed on freshwater organisins during the xval-mer northern than the southern Etlrasian populations of tlle Red- il~onthsof the year." Stock also L'o~indhigh infection rates of necked Grebe, even o11 the wiirtei-ing grounds wllere these several species of lrelmintl~s:90 of 91 of all Iris grebes were two f'c)rms occllr together (Fjelds; 1982b). These dietary iilf'ected by Dicmnokcenicc parclfiorale, 50 of 53 Western ailcl differences presumably af'f'ected at least the proportions of Red-necked grebes by Co~;fluarinJiLrei~?rn,and 59 of 64 Rcd- different specics in the Irelminth coininunities of these two necked and Eared grebes I)y firlricl hiwmia. popt~lationsand between them and that of the Nortl~An~erican The functional relatioilsllips and inicrohabitat distributions Red-necked Grebes. It is also clear that helmiilth cominuni- of the helininths Stock found \yere reported in Stock and ties of grebes on salt-water wintering grountls must dil'f'er I-Iolmcs (1988). From these studies in Alberta, they concluded from those on the fresh-water hrecdii~ggrounds. Parasites (1987a) that these hellninths f'ormed interactiilg communi- acquired from fresh waters in the course of rnigration inay ties. They argued that such coil~inunities"wo-uld be expected also af'fect helmintlr co~~~muiritiesafter arrival at the breeding in species-rich assenrblages of parasites with relatively high grounds. It would be interesting to find out how ecological transmission rates, leading to regular co-occurrence of large character displaceil~entand character release in these and populations of' inany specics" and that "in such a systern, other species pairs of grebes (YjeldsH, 1983a) nlay have affected interspecific interactions would be expected to produce conl- parasite faunas in closely related species of grebe hosts. 11lui1itiesof species adapted not only to their host but also to Bush (1990) discusses soille of' the major conceptual is- other f'requently encountered parasites." A likely result of sues in the study of avian helrnil~thcom~nui~ities and presents such intcractions \ms the predictable occurrence of'thc parasite results from a study ofliclminths of the Willct (Cnlofilrof)hor~~.r species in various sections of the intestine. A conspicuous ac,mif)almalus) which contrast tl~ecommunities Sound in the interaction was the effect of' the large dioecious ccstode, birds on the breeding grounds in Albcrva, with those in birds I)i~~coco.st~.s(z.Y~)PT, on the presence and distribution of other on the coastal wintering grounds. This study provides a model nlcrnbers of the heln~inthcoininunity in Podicrps griseg~~na. for continuing the work of Stock (1985) by obtaining mate- In describing these co~nmunitics,Stock classified the rial of' parasites on the salt-water wintering grounds of the hel~niirtlispecics found in each species of grebe in three species of'grebcs that Stock studied on the bl-ceding groui~ds categories: core species - tliose occur-ring in more than 70 in Alberta and cornparing it with Stock's results. pcrceuc of the birds examined, satellite species - those oc- Other species of grebes which arc likely to have very tiif'- c~u-ringin less than 40 percent, and secondary species - those ferent helminth comn~unitiesare the Pied-billed Grebe, whose in between 40 and 70 percent ofthe birds. 111-ecdingrange extends f'ron~central Canada through the Because the presence of the intestinal parasites in the birds tropics well into ternperate South America, and the Little depends directly on ingestiilg the interrr~ediatehosts of' the Grebc (Tc~clzyDc~/)tusruJicollis), which occurs widely in Eurasia parasites by the birds, the rclative importance of this and of' and Africa and has the greatest n~~mberof digene plus cestode interactions wit11 other palasites after the larval parasites arrive species (84) and total number of parasite species (123) in the bird remain to be determined. reported f'rom any grebe (Table 4). Because grebes exhibit Stock sanlplecl nine lakes of varied sizes and depths but sexual diinorphisn~in bill size, and several in shape as well from only one were all four species of'grebe taken and from (Figure 6), it is likely that these differences inay be reflected six, only a single grebe species was taken. As inigllt be ex- in the diet, and hence in the intestinal parasite faunas. pected, the number of parasite species found in each grebe Stock's inethod of collecting and gathering data would be spccies was related to the nuinber of lalies sarnplcd, as was partic~~lai-lyvaluable in future studies of'grebe helininths to the size of' the sample of each grebe species. Comparisons determine how much thc fat~nasof the salnc grebe species between lalies were not made, presumably because tin~edid vary with sex and age and both locally and regionally. Al- not permit sufficient samples to be taken and analyzed. though extremely time-cons~uining,such studies would be basic In spite of the Sact that all but one of the 12 nailled core to interpretations of possible coevolution of parasite faunas species and two of the six secondary species listed by Stock with the hosts. (1985) are known to occur in Eurasia as well as North America, In order to nlake meaningtill compariso~lsbetween the it is likely that regional differences occur in the n~ake-upof parasite I'a~unasof wiclespread grebe species inhabiting dif- l'crcnt continents or even smaller areas, more basic system- Parasite Collection, through E. P. Hoberg, for permission to cite atic work still needs to be done. For example, Gallimore's specimens in their collcctions. (1964) and Stock's (1985) Sinding the apparent difference The fine original drawings of parasite life cycles wcrc prepared in degree of' host specificity between the North American by John Megallan after illustrations in the following sources: Coven Tatria biretnls Adult worm redrawn from figure in Gulyaev (1990a). ;und European populations of Uiorcoc~~1u.snsprr suggests that Eared Grcbc Farrand (1983). Sigaru from specimc~lin UMMZ. (No difl'erent species may be involved. In addition, ten ofthe species ligurc of the structure of the egg was found.) Figure 1. Petusigernitidus. li)und by Stock were not identified to named species. Eight a. adultworm Beaver (1939a) and Schell (1985),b. Pied-billccl Grebe of tlicsc wcrc hymenolepidids, a group in need ol'a revision. Farrand (1983), c. egg Bcavcr (1939a), d. miracidium, c. planorbid While this detracts but little from Stock's study, it makes snail UMMZ specimen, f. cercaria Bcavcr (1939a), g. bullhead detailed comparisons with similar stludies in other parts of (Ictalur~is)from lifc. Figure 2. Strigrrcfalconis. a adult worm, Schell tlie world dif'ficult or impossible until the proper names can (1985), b. Peregrine Falcon paintings in Brown & Amadon (1968), be ~wovitlcd.As Rarusch (1983) pointed out, "taxonomy, c. egg and d. miracidium (of Cotyluru.\) Olson (1974), c. planorbid snail UMMZ specimen, f. cercaria, Schell (1985). Both Great Crested systematics, and knowledge of cycles remain basic to Grcbcs ancl Peregrine Falcons al-e known to harbor this parasite and investigations involving hclminths." Peregrines al-c known to take this grebe (Uttendiirfcr 1939). Figure The paucity of linown species of ectoparasites on grebes 3. Schi.\tocef)l~.al~i~ssolidus.a. adult worm, b. Red-necked Grebe Farrand docs not malic the study oP their communities worthwhile, (1983), c. egg, and d. coracidimn, Dubinina (1980), Copcpod (Cy- at the ~xesenttime. clops), (T. I. Storer 1943), Stickleback (Gnstrt-ostrzts),Scott & Crossman In summary, the need for new material of'parasites of most (1973). Figure 4. Schistotoenia /(,nuicirr~~s.a. adult worm, Chandler species of birds is great. With the increasing difficulties in (1948), Pied-billed (;rebe Farrand (1983), c. egg and d. dragonfly obtai~iingcollecting permits and the fact that when a host nymph (Arrax,junius) with strobiloccrcoid larva of parasite, Boertje (197.5). Figure 5. Cor)lnosoma st,-r~mo.rum.a. adult worm and c. egg, species becornes extinct, the parasites that depend on it lor Ryzhikov ei ul. (1985), b. Red-necked Grcbc Farrand (1983), d. their existence do also, a concerted effort to link avifaunal amphipod (Panloporcia), Bousfield (1973),California Sealion Peterson surveys with those of thc birds' parasite faunas is sorely needed. and Bartholomew (1967), and adult and young Steelhead Trout (Sulmo Tlills, it is important that ways be found for someone versed gairdnrri) , Scott & Crossman ( 1973). in 111c collection and preservation of parasites, to be part of Special thanks go to Mclis;~D. Ricketts for her caref.ul editing of rcgional surveys of vertebrates. (Clayton & Moore [I997 the manuscript. appendices A, B, and C] and references therein provide ba- sic and detailed "how to" information for this.) It is also im- LITERATURE CITED portant that at least vorlchers ol'the species ol'parasites found be tleposited in repr~tablclong-term collections such as the Abdel-Malek, E. T. 1953. Life history of I'etosiger chandlcri (Trcma- U. S. National Parasite Collection (Lichtenfels et nl. 1992). toda: Echinostomatidae) from the Pied-billed Grebe, Podilj~mbus I do not think it an exaggeration to say that a profitable lifc- porlice~)spodzccps,with some comments on other spccies of Pet(i5iger J. Parasitol. 39:152-157. time of rcscarcl-r could be spent studying the parasites of just Adamson, Martin L. 1987. Pliylogenctic analysis of tlie higher clas- tlic grebes. sification of the Nematoda. Can. J.Zool. 65:1478-1482. Akhumian, K. S. 1966. [On the study of tlie species composition of hclminths of comrnercially hunted and other wild birds in the Armenian SSR.] (In Russian.) Biol. Zhurnal Armcnii, vol. A work of this scope wo~rldhave been impossible without the help 19(11) Nov., pp. 98-104. of 1n;iny specialists. In particular, I have ~relicdon assistance from Alekseev, V. M. & Z. B. Smetanina. 1968. [Nematodes of rish-eat- ~)a~.asitologistsincluding C. Anderson, W. T. Atyeo, C. M. Bartlctt, R. ing birds of Rimsky-Korsakov Islands.] (In Russian.) Gcl'mint. I). 1-1. Clayton, W. 13. (:oil, R. W. Davics,J.A. Fournier, B. B. Georgicv, zhivot. Tikliogo Okcana (Helmintlis of animals of the Pacific N. Hilgi~rtl~,E. P. Hoberg, J.C. Holrncs, A. Jones, J. M. Iiinsclla, J. S. Ocean) 7:97-104. M.ack~cwicz, . ' S. 11. M;irtorclli, S. V. Mironov, P. M. Nollcn, B. M. Allen, J. A. 1876. In: A. Agassiz and S. W. Garman. Exploration of OConnor, li. D. Pricc, li. L. Rat~scli,S. C. Schcll, J. L. Staton, T. M. Stock, (:. A. Sutton dc Licitra, M. Ulmcr, ancll. C. Walker, scvcr;~loC 1,ake Titicaca 111. - I.ist of mammals and birds. Bull. Mus. Comp. wlio~nchccltctl all or parts ofthc manuscript and prevented my making Zool. 3:349-359. nulrrcrotls crl-ors both large and small. I am also deeply cndebted to American Ornithologists' Union. 1985. Thirty-CiCth supplement to F.. 1'. Moberg, J. C. Molmcs, and J. S. Mackicicz fbl- thcir kind ancl the American Ornithologists' Union Check-list of North Ameri- IIcI~SLIIrc\~iews of tlic manuscript, and to E. P. Hoberg and J. M. can Birds. Auk 102:680-686. Iiinscll;~Sot- iclcntifying ant1 checking identilications in the U. S. Anderson, R. C. 1988. Nematode transmission patterns. J. Parasitol. N;~tionall';tr;~sitc (:ollcction and thc H. W. Maliter 1,ahoratory. I 74:30-45. havc bccn aided I,y biologists and specialists in other groups including Anderson, K.C. 1992. Nematode parasites of vertebrates; their dc- R. M. Uailcy,J. U. Burch, H. 1). Cameron, T.J.Cohn, B. S. Dyer, B. A. velopment arid transmission. xiii+ 578 pp. (:. A. B. Intcrnation;~l. II;~zlctt,G. S. I-I;rmmond,J. li. Jel~l,Jr., M. F. O'Bricn, and G. E. Anderson, R. C. & C. M. Bartlett. 1994. Ephemerality and Schncirlcr. J. I<. Coolcy, D. Ciszck and G. S. Hammond preparcd reproductive senescence in avian filarioids. Parasitol. Today 10 Lhc compulcr ;ni;rlyscs. In spite of this generous assistance, there (1):33-35. prol)al)ly still will be errors. For these, I must accept rcsponsibility. Anderson, R. C. & P. L. Wong. 1981. Redescription of Cosmocef~l~ulzr.~ 1). W. Nelson tr;rnslatetl material in Russian, and 0.Z. Scllinger that obvclat~cs (Crcplin, 1825) (Nematoda: Acuarioidca) from Larus in Scrho-(:roa~ian.Special thanks arc clue to the staff' ofthe University dr1awarc.n~~~Ord (Laridae). Can. J. Zool. 59:1897-1902. ofMichig;m Natural Sciences and Museums libraries and Interlibrary Anderson, R. C. & P. L. Wong. 1982. The transmission and Lo;rn Department for finding and obtaining references, and to the development of Pararunria adl~nca(Crcplin, 1846) (Nematoda: I-liu-oltlW. M;~ntcrI,abo~.atory oSPamsitolo~y, University of Nebraska Acuarioidea) of gulls (Laridae). ibid. 60:3092-3104. St;~tcMLISCLIIKI, tl11.011gll S. Sterner, and the United States National Ash, J. S. 1960. A st~~dyof the Mallophag;~ofbil-ds with particular 25:269-275. refcrcnce to their ecology. Ibis 102:9:3-110. fie.n\c . , I, 1'. (;. 193911. Tl~c~rrorphology irnd lilk Iiistory ot I'\ilo.\lomum Bacr, J. C;. 1940. So~ncavian tapc\vo~-~nsIro~n Antigua. Paritsitol. o~rdo~rnrPrice, 1931 (TI-cmatoda:Psilosto~nidae). ibid. 25:383- 32:174-197. 393. B;~cr.,J. (:. 1957. Repartition ct cndC~nicitddcs ccstodes cher les ficavcr, 1'. C. 1941. Tlre life history of I:'clri~~oc.ha,srrrusdonnldso~ri 11. reptiles, oiscal~x,ct ~nammifi.rcs.First sy~nposiumon host sp., a trematode (Ecliinostomatidae) from the l'iccl-billctl Grebe. specificity among parasites of vcrtcbl-arcs. Inst. Zool., Univ. ibid. 27:347-355. Ncuchatc.l. Proc. 1ntcrn;tt. Union Biol. Sci. Scl-. B, no. 32, pp. BCdartl, .J. 1969. Adaptive Radiation in Alcidac. Ibis 11 1:189-198. 270-292. Behrstock, R. A. 1981. 1'1-cy-inducedliiortalily ofa Pied-billed Grcbc. R;undorf, I-I. 1970. 1)er Zrvrrgtauclrcr (7iic-Iry6~~1111~.sruJirollis [Pallasl). Western Birds 12:183-1 84. Die Ncuc Brchm-Biicherci. A. Zicmsen Vcl-lag. Wittenl~rrg Bittncr, H. Sc C. Spre1111.1928. Trematodes. Saug\vi~rmcr,1,icfcl-ung l~utherstaclt. 27, Tril 5. Pp. 5.1-5.13:'P. In: 1'. Sclrulzc ecl. Biologic drr Tiere B;utlctt, C. M. 1992. (:old-hardiness in I'~l~ti/zi,sJiilzc.ner~lrn/, (Ncn~it- 1)eutschlands. Borntl-acgcl- Rros. Berlin. rod;\: Filarioidea), a parasite of the ankles of' I'ulirrc cc~nr>ricalrn Blake, h. 1<. 1977. Manual olNeotropica1 Birds. Univ. Chiciljio l'rcss, (Aves).J. Pill-asitol. 78: 138-139. Chic;~goand 1,olldon. Bartlctt, <:. M. & R. (:. Anderson. 1987. I'PIP~I/IISfitlirne~n~rnr Bla~ikespoor,H. 1). 1974. Host-induced variation in P1r~g;orc.hi.s~Loblpi (Ncm;rtoda: Fil;~rioidca) of coots (c;~-uil'o~-rncs)and grrhes Park, 1936 (Plagiorclriidae: Trcmatoda). Anrcr. Midl. Nat. 92:415- (Podicipcdiformcs): skin-i~il~abitingnlicrofilariac and devclop- 433. ~licncin Mallophap. Can. J. Zool. 65:2803-2812. Bocl~eliski,Z. M. 1994. The colnp;~r;~tivcostcology olgrcl~cs(Aves: Bartlett, C. M. Sc R. C. Anderson. 1989a. Sornc observations on Podicipediformcs) and its systematic i~nplicatio~is.Act;\ zool. hzrrdomnropori l~ilosrrm(Anihlycera: Menoponidae), the lo~lscvcc- criicov. 37(1):191-346. tor of I'c~lc~c.i/rts,f~tlcc~c~~~~~tr(Nematoda: Filarioidea) of coots, I"c~lic.cc Boddeke, 12. 1960. Tlrc lik history olI'~-os/h/~gor~imu,sourrlu, Kr~doll~lri. nrn/~ric.ci~~n(Aves; Gruifol.nlcs). ibid. 67: 1328-1 331. 1. Experirrrcnts in bil-ds. TI-op.gcogr. Med. 12:2(53-292. Bartlctt, C. M. & R. C. Anderson. 198913. Mallopliagan vectors and Bocrtjc, S. B. 1974. 1,ilc cycle ;~ndhost-parasite relationsllips of tllc avian Glarioids: new subspecies of I'(,l(,cilris Jirlir(~ert/r.nc.(Ncnia- Schistotrcmin trnuicirru~(Cestoda: Amabiliidac). PI-oc.I>o~~isiana tod:~:Fil;u-ioidc;~) in sy~npatricNorth Arnrricari hosts, with dc- Acad. Sci. 37:89-103. velopmrnt, cpizootiology, and patliogenesis of the parabite in Bocl-tje, S. B. 1975. Developmental stages anti strohiloccrcoid of I"~rlic.rcnrr~(~r-ic.crrrrr (Avcs). iljicl. 67:2821-283:'~. Schi.\totcr~ninIPI~II~(~T~UJ (Ccstotla: An1;tbiliidac). ibid. 38:52-(59. Bill-tlctt, (;. M. 8c E. (;. GI-eincr. l98(i. A revision of I'I~~PI.~/~L.~Railliet Borgarcnko, I>. F. 8c V. D. (;ulyaev.l990. [On niorpllology of type and Henry, 1910 (Filarioidea, Dirofilariini~c)ant1 cvidcncc fol- species of the genus ~o~c~uxrle~~is(Ccstoda, Scliistotaeniinar)1. the "c;~pt~~re"by rnarn~nals of f'ilarioids fi-on1 birds. Bull. MLIS. (In Rllssian.) Pal-azitologiya (Leningr.) 24::150-353. n;rtn. Mist. nat., I'aris Sect. A. Zool. Riol. Ecol. Anim. Scl-. 4, No. Borgarcnko, L. I?. Sc V. D. Gulyacv. 1991. [Two new ;lmabiliid cestodes 8, pp. 47-99. El-on1 gl-cl)cs ill Tad~hikistan.](In Russian witlr English summa~-y.) Bartoli. 1'. 1989. Digcnctic 11-cm;~todcs;IS hio-indicators for Ycllow- Izvest. Sib. Otd. Akad, Nauk SSSR. Sib. hiol. ~h~u-nal1991 (1):44- lcggccl Gulls in (hrsica (\Vestern Mediterranean). In: Aguila~; 48. J. S., X. Morihilillii~,and A. M. P;~tcrson,cds. Status ;ind consel-- HOI-garenko,L. F., L. P. Spasskaya Sc A. A. Spassky. 1972. (Ccstodes v;rtion of seabirds ecogcoglxphy and Mcditcrrancan action plan. ofthr genus 7irlrirr intesting waterbirds of Tadzhikistan.) Izvest. Madrid: Society of Spanish Ornithology, 11)811:251-259. Akad. Ni~uktadzliik. SSR 1972(4):53-.57. (111 Rl~ssia~rwith Tadzliik B;rrtonek, J. C. & D. I,. Tr;~ugcr.1975. 1,ccch (Hirudinca) infcsta- suninlary.) tions among waterfowl ncal-Yellowknife, Northwest Teri-itol-ics. Bousfield, E. I,. 1973. Shallow-water Calnmaridcan Amphipoda of (:an. Field-Nat. 89:234-243. Nc~vEngland. (:omstock Pr~hl.Associates, (:ornell Univ. Press. B>u.118,V. & T. P. Sel-gcjcva. 1990a. (:apilla~-iidspal-asitic in hil-ds in Ithaca and London. thc Palaearctic Region (1) (;elins Co/)illnria.Prirod. Price ~.\tavu Boycl, W. S. Sc J. 12. Jelil, JI-. 1998. Estimating tl~eabunda~ice of Ccsk. Altatl. VCtl BrnC 23 (1980). No. 3:l-50. Eareti Grebes (Porlic.p/).\ nipricollis) on Mono I.akc, California, by Bar118, V. & T, P. Scrgcjeva. 1990b. (:apillariids parasitic in birds aerial photogri~phy.(:olonial Waterbil-ds, 21 (2):23(i-2/11 in the P;ll;tearctic Region (2) Genera Eucolpus and I?c.hinoc.ol~u\. liravo-Hollis, M. 1969. Prtnsigc,r (N/,of~(,la.\igor)pteutlonc,oc.omrn,w /J;c/ ibid. 23. (1 989). No. 6:l-47. sp. nov. (Echinosto~natidacI'ochc, 1926) del intestine tie Har~lE,V. & T. P. Scrgcjcva. 19110~.Capillariicls parasitic in birds Ar'chmo/~horc~coc.c.irl~nlnli.\ (Lawrence) de Bahia tlc Todos Santos, in the Pi~lacilrctic12cgion (3) Genus Hnrrrscn/)~llarin.ihid. Baja Cirlithrnia. An. Inst. Biol. Univ. Nal. Aut6n. Mexico 40, Scr. 24. (1990). No. 10:l-53. Zool. (1):15-20, 1 pl. BaruK, V., T. 1'. Sergetileva, M. D. Sorii~i& I<. M. Ry~hikov 1978. Brglc~,1. 1976. [I:'chinochasm~~.\(Lchinoc.hnsmli\) brlroc./~l)hnlus I-lclminths offish-eating birds of the Palearctic Region 1. Nclna- (Idinstow, 1873) and L:'c-hinoc-lrcc~mus(I:'cltinoc.hnsmzts)rlielte~~i toda. 318 pp. B. RySavy. iinrl K. M. Ryzliikov Eds. Dr W.,Junk, b. Issaitsclrikoff, 1927 two species of cchinostomatids v. Publ., The Hague. (Echinostornatidac Ilietz, 1909) in some hil-ds in Slovenia.] (In D~I~II?,V. & D. Zitjicck. 1967. Parasitic Nc~natodcsof Birds of thc Scrbo-CI-oatian.) Zborn. 1)iotechn. fak. Univ. Lj~~bljana13:93- Order Colymbif'or~ncsin Czechoslovakia. Folia Parasitol (Pnha) 98. 14:73-85. Brglcz, ,J. 1977. [Contribution to tl~eknowledge of. distribution Baycr, R. D. 1980. Birds feeding on herring eggs at the Yaquina and patliogcnicity of Acrrn/hoc.rl)hc~lrr,family I'olymorj~lritlneMcycr, Estuary, Oregon. Col~dor82:193-1 98. 1931, in birds in Slovcnid. (In Sr~-bo-(:roatian.)ihid. 14(2):173- Bc;lvcr., P. C. 1937. Expcri~ncntalstudies on I:'c.lrirro~/orncrr-e7)ol1tlzcrrr 180. (F~.oclich),a flukc from birds and manim;~ls.Illinois Biol. Monogn BI-ooks, D. It., S. M. Bandoni, C. A. Macdonald & R. T. O'Grady. 15:l-96. 1989. Aspects ofthe pliylogeny of tlrc Trc~natodaRudolphi, 1808 Beaver, P. (:. 1939a. Tile ~no~-phologyand life histol-y ol Prtcctigrr (Platyhelminthcs: Ccrcotncria). Can. J. Zool. li7:2(509-2624 nilidri~[.inton (Trc~natoda:Echinostornatidac). ,I. Pal-;rsitol. Brooks, 1). 12. 8c D. A. McLcnn;rn. 1993. Parascript. P;rrasitcs ant1 the I;~ngn;~gcof evolution. x + 429 pp. Smillisonian Inst. I'ress. Coil, W. I-I. 1984. Studies on the devcloprnent of Dioecoce.~/~u.snrotylus Wi~sliington;rnd London. (Ccstoda) with emphasis on the scanning electron microscopy l\rooks, D. R., I<. T. O'G~-;ldy& D. R. Glen. 1985. Phylogenetic of cmbryogenesis. Proc. Hcln~intliol.Soc. Wasli. 51:113-120. ;~n;rlysisof tl~cDigcnc;~ (IPlatyhclminthcs: Ccrcomeria) with Cooper, A. & D. Penny. 1997. Mass survival of birds across the conr~ncn(s~II their- adaptive radiation. Can. J. Zool. (il:411-443. Cretaceous-Tertiary boundary: molecular evidence. Science I%row~~,L. & D. Am;iclon. 1968. Eagles, Hawks and Falcons of the 275:1109-1113. Worltl. Vol. 2. Mc(;l-aw Book Co., New Y~I-k. Cracrafl, J. 1982. Phylogenetic relationships and monoplryly of I',ush, A. 0.1990. I-Iclminth conrnrunities in ;~vi;~nhosts: dctermi- loons, grebes, and Iiesperornithifoi-m birds, with comments 011 Il;tnts of pattern. l'p 197-232, In: Parasite communities: pat- the early history of birds. Syst. Zool. 31:35-56. terns a~~dPI-occsscs. G. Esch, A. Bt~sh,andJ. Aho, eds. Chapman Cramp, S. (Chief Ed.). (1977). Handbook of the birds of Europe, i~nd1-1;111, Lontlori and New York. the Middle East and North Africa. The birds of the western I\r~sh,A. O.,J. M. Alio & (:. R. I I-Iobcrg, E. P., 1). 11. BI-oolts & D. Sicgcl-Caksey. 1997. Host-parasite Jones, A. 1994. Family 1)ioccoccstidae Southwell, 1930. Pp. 391- co-speciation: history, principles, and PI-cspccts.I'p. 212-235. h: 398 In:Iihalil, 1.. F., A. Jones, and R. A. Bray (cds.). Kcys to the (:layton, D. I-I., and J. Moore, (cds.). Host-parasite Evolution: cestoclc parasites of vc~.tcbratcs.CAB Intct-national. Wallingford, Gcncr.;~lPrinciples ant1 Avian Models. Oxford Univ. Prcss, Oxford, Oxon. U. I<. Ncw Yorli, Tokyo. Joycux, Ch. &,I. G. Baer. 1936. Fa~unedc FI-ancc.Paris. SO. Cestodes, I-lobcrg, 1':. P., S. L. Gartlncr & R. A. (:ampbell. 1999. Systerliatics 61 3 pp. ofthc Euccstocl;~:advances toward a new ~)liylogerrcticpar;~cligm, Joycux, C:h. & J. G. Baer. 1943. Sur quclqucs l~cl~nintl~esdu Maroc. ;rnd obscrv;~tionson the c;~rlydivel-sific;ltion of tapeworms and Note prCliniinaire. Bull. Soc. Pathol. Exot. 36:86-88. vcrtchratcs. Sys~.l';~rasi~ol. 42: 1-12. Joyeux, (;h. & J.G. Bitel-. 1950. Sur quelques csp6ces nouvellcs 011 IHobc.rg, 1':. l'., A.,joncs & li. A. Bray. 1999. Plrylogcnctic analysis pen connucs clu genre Hjmc,rrolul,i.\ Weinland, 1858. Bull. Soc. i11110ngthe li~niilicsol'thc Cyclopllyllidc;~(Eucestoda) based on Neuchatcloisc Sci. Nat. 73 (ser. 3):51-70. co~np;~r;~tivcnlorpliology, with new hypothcscs for co-evolutiorl Joyc~~x,Ch. & ,J. Gaucl. 1945. Rec1rc1-chcs I~clmintliologiques in vcrtcbr;~tcs. Syst. l'arasitol. 42:51-73. Marocaines. Arcl~iv.Inst. Paste~u-Maroc. 3(4):111-143. I-loll'man, C. I,. 1967. I'arasitcs of North A~nericanSrcsl~w;~tcr fishes. Kanev, 1. 1994. Life-cyclr, delimitation and rcclcscription of Llniv. (:alif'. Prcss, Bcrkclcy and I.os Angclcs. ix + 486 pp. Lc.liinoctomn ~CTIO~I~I/IIII(FI-oclich, 1802) (Trernatoda: I-lopkins, G.I-I. E. & T. Clay. 1952. A check list of the genera and Lchinostomatidae). Syst. I'al-asitol. 28:125-144. sl)(:cics of M;~lloph;~ga.RI-it. Mus. (Nat. Hist), London. Kanev, I., P. Nollcn, I. Vassilcv, V. lIadcv & V. 1)irnelrov. 1993. I-Iutlson, G. 1.1. 1937. Studies on the ~n~~sclesof the pelvic appcncl- Rcclcscr-iption of I'hilophlhnltntts lrccipr/7r.s (Rudolphi, 1819) ;rgc in bircls. Amcr. Midl;rntl Nar. 18(1). pi). 1.108. (Trenratoda: Pl~ilopl~tlrallrridac)wit11 a discussion of'its identity I-IufS~uan,,J.E. & B. Fried. 1990. Echinostoma and l'.clii~rosto~lliasis. and clraracteristics. Ann. Natul-lrist. Mus. M'icn 94/95B:11-34. Atlvanccs in Pal-;~sitology29:215-269. Kcllogg, V. I.. 1896. Nc\v Mallopl~aga,I, with special rcfcrcnce to I-lugghi~rs,E. J. 1954a. L.il'c histol-y of ;I strigcid trematode, a collection made from ~naritimcbirds of the Bay of Monterey, I-lvt/~rottro~l,cr/rilobn (Kutlolphi. 1819) I.1it7, 1931. I. Egg ancl California. Proc. Calif. Acad. Sci., scl-. 2:31-168. mir;~citlium.TI-ans Amel-. Microscop. Soc. 73: 1-15. Lcettle, P. R. 1974. Aqi.~a?iir.m~lsuuslralis 11. sp. (Mallophaga: l-lugghins, 1.:. J. 19540. Life Iristory of a stl-igcid trcnratodc, I'hilopteridae) lronr the New Zcalancl l)abchick, Podic-eps l-l~~.~l~t~o?ttor/~/~~~~lrilo/)n (liutlolphi, 1819) I.utz, 1931. 11. Sporocyst rufofj~c.ius.New Zcaland J.Zool. 1:337-340. throl~ghatlult. ibitl. 73:221-236. Iihalila, R. 1972. Studies on Sc/~i.slosomulidaeLooss, 1899 (fiema- T-Iy~n;ln,I.. 1-1. 1!)51;1. The Invcl-tcbl-;~tcs.Vol. 2. Platyliclrnintl~~s lorla) of aquatic birds of I'oland. I. 011 tllc life cycle ol'nilhnrziella ;tnd Rhynchococl;~,The acoclon~;rtcBilatcl-ia. vii + 550 pp. fjolonitn Kocvalewski, 1895, will1 a discussion 01. the subLtmily McCr;i\v-I-Iill, Nclv York. Bill~rlrzi~llitznrPrice, 1929. Acta Parasitol Polonica, 20:343-365. I-I~III~III,I,. H. 195111. The Invcrtcbr;~tcs.Vol. 3. Acanthoccph;~la, Khalil, L. F., A. Jones 8c R. A. BI-ay. Eds. 1994. Kcys to the ccstodc Aschclminthcs, and lintoprocta. The pseudocoelomate 13ilatcl-ia, p;~rasitcsof vcrtchratcs. xiiit751 pp. CAB Intel-national. vii + 572 pp. McCr;~w-I-Till,New York. Wallingford, Oxon, U. I<. Ilts;~nov& l)ikambacv;~.11182. [Material for a st~idyon infection of Iiholthlova, 1. 6. 1978. [A taxonomic survey of acanthoccphalans piscivoro~~sbil-tls wit11 ncmatodcs in Kirgizia.] ILV.Akad. Nauk in bil-ds of the USSII.] (In Kussian.) Trudy Gel'mint. Lab. 28:12I- I trcm;~todcs.XXX. 1,ifc cyclc of I'cln.srger ?I07~/,11ldecimI,ut~, 11128. Zool. 63:259-263. Proc. 1-lclminthol. Soc. Washington 39:162-168. l'cters, J. L. 1931. Check-list of birds of the world. Vol. 2. Harvard N;tsil., 1'. & ,J. V. Scor~a.1968. Studies on fresh~vaterlarval Univ. Prcss, Cambrid~c.xvii + 401 pp. trcm;t~odes.XVIII. Tlle life cycle of Stefilrnrro/~rul.cr rlrntirulnla Peterson, R. S. & G. A. Bartholomew. 1967. Tlic Natul-al History (Rudolplii, 1802) Odhncr, 1910. Zcitschr. f. Parasitenk. 30:134- and Behavior of the California Sea Lion. Spec. Publ. Amcr. Soc. 148. Marnmalogists. No. 1. xi + 79 pp. Nassi, I-I. 1980. Don~lCcexp6rimentalcs sur Ic cyclc biologique Petrova, I<. 1978. [Studies on the helminth fauna in wild bil-ds of dc l1c~/n,si~/~rrc~rihberr,si.\ ti. sp. (Trcmatocla: Echinostomalidae) para- Thrace. 3. Ccstodes.] I p.'11 ..nsltcs .' of Tachybaptlis nouaeltollandiae 7ylodelphy.s conifern (Mchlis, 1846) 1)IGENES 7)loc/~lf~hy.\(,xcaunin (liudolphi, 1803) ~~~~:l.o~:ob:1.lll:\l~. S I l C;,\~II,\I~II\SIIIII\I:, Pnramo?zostomum raeti Srnitli & Hickman, 1983 Ribeiroia o'n,datrne (Price, 1931) ~YCI.OCOEI,ID.A~~ E(:IIINOSI.~R.III)~\I,. Cor/rof)yrurn jnt,nschi (Johnston & Simpson, 1940) Ecliir~~orhrrsrnristlorrtilrlso17i Rcavcr, 1941 Psr~.osrohr~n,\~ P~liisig~rrlin7icll/~ri Abdel-Malek, 1952 I'silochasnius oxyurus (Creplin, 1825) P~/rrrigor,/'loridusPrcmvati, 1968 ECIIINOSTO~IID-\E I'plnsifi-pr II~/~~z/JI.inton, 1928 Prtasiger oustralis Johnston & Angel, 1941 STRIGFII).+F Cigcr~tlul~illt~cirziclelongcctci (Brackett, 1940) Schwccrlrilrc~mccparzdubi (Pande, 1939) MI(:I Par asltes of Poliocephalus rufopectus LICE Sclti.stolrrr~nii~mncrocirrut (:hilndlcr, 1948 1'1311 OI'ILRIL? 11 Schi.\totnrn,iir .\colopenrlro (Diesing, 1856) Aquanirrnus auctralic ICcttlc, 1974 Srlii.stolnc:~i,ioI~~nicicirrzis Chandler, 1948 Yictrici rl~rod~~rrrcnnlhnOlsen, 1939 I-~Y~II:N~I,I:.I~II)II~,\I< Parasites of Podicephorus major Con,/lrrnr-ia ,furcv/,ra (ICrahhc, 1869) DICENES I,obnlol'/ris lobttlirln (Mayhew, 1925) ECIIIN~SI obr~r),\t ACANTI-IOCEPI-IAIANS Me.sorchis nrg~ntinm.ris(Sutton, Lunaschi & Topa, 1982) I'olymorpliu.\ rnc.yc,ri I,l~ndstriinl,1942 iMrso7-chis rlenticulafus (Rutlolphi, 1802) NEMATODES Mrsorclris pocliripei (Etchcgoin 8c Martorelli, 1997) Parasites of Podiceps auritus IIICENES No roc:(>IYI.II)AI~ (~I.OSS~~'IIONIIL~I\I: ~Vuluto/ylu.\cr/teirtratri~ (Rudolphi, 1809) Y'lii~romyzo7i "orcirlrrilnli\ " (Vcrrill, 1874) CA.IIl,\tbr,\srlu:\e r.Ili,~~romyzon "lriz~ri(ir~"l~avics & Ooshuizen, 1993 Ribeiroici ondatrar (Price, 1931) MITES E(:llrNOS~rOb~InhE ~~~\hllNOSlOl~~~I1~~\l 1:'chinochasmus donaldsoni Beaver, 1941 I'odirijr/~tlico/,/e,nm~rictcnu.r I>ombcrt, I 1-IK ~?~/I~III(,I~o.\/~.\\I\~JIJI(I (Dicsing, 1861) (;ry/)loc.ofj~lrli~rgrro (Cs-cplin, 1825) A(:l1.\1<111>.-\1 ~<,NI(:oI.II),\F (:o\~ero(~plrrrltr\oho~lrr/ri.\ ((:I-cplin, 1825) H~~ric.oln/~ingtris (Mchlis in <:rcplin, 18/16) I(e1~ieruricr ci~rc.r~rrr/cr(Rudolphi, 1819) 1'1<0S l'llO~rON1~lIl)~\l~ I'crrrrtucrricl cltl7rirtn ((:rcplin, 1846) I-'ro,s/hogoreirntr,\ c.elrrrotrrs (Rudolphi, 1809) Sle-o/)torcrr-cr rl-crssic.oucln (C;rcplin, 1829) 17.11(:0 I\I.II)AI< S/~-(,/~/otrrrcrrc,c-/cr (I.instow, 1879) L'IL~.o~J/Pc.oh?ei Skl:j;lbin, 1924 S~l1~7l(l/-i(ldf't Ol(l/(l ((:r>ll~l,1927) Ec/ro/ylr~hcrsscrlli I'ricc, 1990 oN<~l10<.E1<~:11~.\~ CESTODES Ppl(,c.ilzr~JIIII((IP(I/I~IP (Uiesi~ig, 1861) l)~~,~lv~.l.o~roI.III 7. Ligrrlrr rn/c~.slir~crlit(I.iri~iacris, 1758) Ilr(~~o~npzo~r"(I-rzo~rcrer," l)a\rics & Oosthui~cn,1993 Scl~i.\toc.r,phrrlre.\ prrrrgitir l)ul,i~iina, 1959 MITES Sclri.s/oc.(~/~/enlr~.\solit1re.s (Mucllcr, 1776) PI I1 OSl:Nll>-\I: TICr1<:\15o ~III ilpnlrmon grncilis (Rudolphi, 1819) fchllryocotyl~~,-usr7-raticus (Rudolphi, 1809) A~I~O.SPI/)P,IISt~ro~goz~oyi Supryaga, 1965 Ichfhyocolylur~~~plntyrc.j,Anlus (Creplin, 182.5) Szidat, Tic I I<,\~~II,I For case in Lintling species in the general acco~mtsof parasites and ofgrebes in the lists of their prey species and parasites. page n1unhcrs for these are in italics . For the last two. the lower nurnber is for the list ofprey species and the higher number is for the list of parasites of the grebe species . The first page of each species account for each family of parasites is also given in italics . Page ntunbcrs Por other entries are in plain text. Sllbjects in the table ofcontents. and narncs ofspecies ofprey and ofintermediate hosts arc not intlexcd . The data on the last two are in analyzablc forrn on the web (see p . 6). def. = definition. fig . = figure . Acanthoccphala (acanthoccphalans) ...... 43. 47 bahli chambwlini ...... 61 acantliella. dcl: ...... 26 bahli group ...... 61 acanthor larva. del: ...... 26 bucoinfish.i ...... 37 ac:unthor larva. fig ...... 27 chambmlini ...... 37 copulatory cap ...... 26 colymbinus ...... 3 7 60 cystacanth. dcf:...... 26 colyvabi17~usgroup ...... 61 sp ...... 28 emmsoni ...... 36. 61 proboscis ...... 47 occidenlalis ...... 36 ... Ac;~ri(see mites) podrcz/~z.s...... 37 Ac;rriI'ornles ...... 34 podil~vnhu.r...... 37 Acoleata ...... 50 re~ncin.alu.,...... 37 Acoleidae ...... 25 Arhythmorhpch.u s (see Southwrllin.a h.isl,ida) Acuariictac ...... 31 arthropods ...... 4 A~c.I~ttlo/~lrorc~.r...... 42. 43. 48. 59 Ascaridida (ascaridoids) ...... 29, 30 clrrrl{ii...... 41. 48. 51 Alriophallophorus coxiell(~e...... I6 clec?kii. bill lhrln. lig ...... 44 auks (see also Alcidae) ...... 5 oc.ciderrl~clis...... 18. 41. 48. 50. 51. 55. 56. 57. 61. 64. 82 Australia ...... 60 i\kolo(. nicr ...... 45. 61 Auio.rtll,c.n.s mo.,gouojli ...... 31, 5 1 Alcidae (alcids) ...... 2. 48. 45. 49. 62 Bmruscc~f)ill~~riacarbonis ...... 29 A~nabiliid;lc(amabiliids) .... 3. 20. 49. 50. 51. 52. 53. 55. 56. 59 mwgi ...... 29 proglolticls. lateral projections on ...... 53 obsiflula ...... 29 .... A~nblycer;~.(Pht11iraptcr.a) food ...... 36. 60 podrc?pzIzs ...... 30 Atniclostomidae ...... 30 ryjilzo7)i ...... 30 A.rr.ir/o.slonrumcrn.sc.r.is ...... 30 bedbugs (Cimicidae)...... 48 licn~...... 30 Bering Land Bridge ...... 61 rcrilli~li(see A . ficlic.crc,) Biglandalrium bigl(~ndntrium...... 23 .~n.lci~.orilousIislles ...... 4. 5. 26. 62 Bilharziell(~polonica ...... 12 Analgidae ...... 34 biodiversity studies ...... 49 At?ax ...... 54 black-spot disease (see Crj~tocotylrlingi~cc) ...... 16 .j1117.iei.s.nymph. lig ...... 21 Ellre Mihale (Bala~n.optm musculus) ...... 52 jun.i.u s ...... 3. 47. 52. 55 bothria (in Pscudophylliclea) ...... 47 Anrl~c~ccmlhn...... 26 bothridia (in Tetrabothriidae) ...... 47 ttz(. r~i...... 26 California Sea Lion (ZrcloFhus calzfomianus), fig ...... 27 p11r~lnt~oeo~rrc.i~~...... 26 C(~f)illariaanalis ...... 30 Anisaliidac ...... 30 mich.igclnen.sis ...... 30 Anisoptera (cll.agonllies) ...... 20. 56 obsiignaln (see Baruscapillaricc o.) anrlclid worms ...... 4 fiacl~~~dermn(scc I.; IICO~PIISCO~Z~O~~IL.~) A17orrtolnonicl 1zydroc.h~lidonis(see Lig(c Cncomnica) sp ...... 30 A/)(L~P.~orr pc.ili.s ...... 14 Capillariidae ...... 29 Iruoni.\ (scc Schwccrtzitrne Fandubi) Capillariinae ...... 50 A/)horyngo.slrIg(!acot'~2.1 I ...... 14 Chinema Dilqoc!sar ...... 33 A/~lopctrclk.si.s...... 24. 25 catadromous fishes ...... 4. 62 cr(i.ssiro.vlri.s...... 2-3 Cathacmasiidae ...... 8 bli/i)~~tri.s ...... 23 Cnloptrophorus .remz.l,almalu~ ...... 64 .jr rciy m ...... 23 Cephalogonimidac ...... 17 lnri.n.cl...... 23 Cekhalogonirnus sp ...... 17 Aj)o/~lrnll.ci.s br(q,is ...... 16 Crrcaria elort.gala (see Gignnlobilharzia P.) . . .tt~.e~~ltbtt~gi...... 15 helurticn (see Diplostomurn .s~)a~hnceum) Apcc7ri~ttru.s...... 36. 49. 60. 61. 62 Cwcan'oides humbergari ...... 16 crrtc~ricclnu.~...... 3 7 cestodes, asexual reproduction. intermediate host ...... 43. 50 cr~c~.str(ili.s...... 7 6 1 damage to host ...... 62 bnhli ...... 37 life cycles ...... 18 8.1 M~sr. PURL . Mua . ZOOL..UNIV . MICH.. NO . 188 . . proglottid ...... 18 /lrD~lllform~.s...... 14 rostelltun ...... 47 m(~oiit~.\(see Ic.htIz~1oc.o~y11~r1isj)il~crI%~~) scolex ...... 18 p1ntycuf)hnlu.scommunis ...... 15 suckers ...... 47 sp ...... 14 chiggers (mites) ...... 34 Cryj)toc.o/~~lc~c.onc.nucr ...... 16 Chironomidae ...... 46 li?zg?tn ...... 16 C;hocrnotcr~n.in (see l'crricl(.,-olneni porosn) Cyalhocolylr prt~.s.sicn...... 13 (:hrysomelidae ...... 5 tr$.nnrrmt~...... 13 cladocerans (Crtistacea) ...... 4 (:yathocohlidac ...... 13 Cleie1ognicr ...... 25 Cyclocoelicl;le ...... X (;/(9si~rte(see Thcwrnyzon) Cyclopl~yllidca...... 47, 50 (:linostonlidac ...... 12 cyclopids (copcpods) ...... 56 Clino.slo,r~ru.rtrco~r~plmnc~lzlrn ...... 12 ($clo/).s, fig ...... 19 plr. silkurn ...... 12 damselflies (scc Zygoptcra) C:lonco/n~'t~inrt~rgnlop.~ ...... 23 daughter cysticel-coids (see 7i?/rjn vrn1~nti.s) Colpocc~[)hnlzcm(see I'.crudornrn,oj)on(1oli.u tn) I)rcor~~nri~(see S~ln.runricL d~corcrln) Colymbus cl.sicclicu.s (see Cclvia clrt.tiec~and I'oclic~j).\ 01~rilzis)...... demography (Amabiliidae & Dioecocestidac) ...... 52 ...... 14, 55 /)en.rl~tohilh.(~zic a~zatinnrum (scc L). pulvc.rz~lrnl(r) nigric.nn.s (see l'odic(9s cuuriku~)...... 12 fiulvn-ul. 17ln ...... 12 Co~ni.s1i..s sp ...... 35 diaptolnids (copepods) ...... 56 Conjttinricc ...... 23 Dicmnoln~~zzcc...... 25 cerpilkrri.~...... 2 3 coronzrla ...... 4 24 cnj)illnroidr.s (see (.. cuj)i(,illar.is) /)nrn/~omlo...... 24, 57, 64 ./ii.~'cifircr ...... 2.3, 24, 52, (54 sp. c)l Gnllimorc (1964) (sec 1). /)arc~por(e/c.) jcc/)onicce ...... 24 digenes (digcllctic tre~natodes)...... 43, 49, 50, 62 .tnul/islr.inlo...... 24 ccrcaria ...... 7 11 . sp . Vasilcva, Georgiev & Genov ...... 24 mcsocercarial scaqe ...... 8 poclici/)717.n ...... 24 rnecacercaria ...... 7 . . sp ...... 24 miracld~~~nl...... 7 .s/tct.ssliii (see C. potlici)intr) I-edkn...... 7 (~onlrercaoclrrr~...... 29, 50 sporocysts ...... 7 an rlrrsmri ...... 30 L)igmmmc~intrr~-u/)ta ...... 18 rt~icroc.(.j,hnlumtn...... 30, 5 1 Dilepididae (dilepiclids)...... 23. 56 ~rrirropoej~ille~~~u~~t~...... 30 sp ...... 23 n.elr.li (scc C: . ovc~le) l)i~norf,hoca~zlhu.s(see C)nJlucrrie~spp.) ...... 23. 24 O~JNIP...... 30, 5 1 lli~cto~hymatidae...... 29 /)orlic.ij)iti~(see C. ovnlr) Dioccoccstidac ...... 20 fi~-eceskrinlzrn~...... 30 strobilocercoid ...... 20 qu~nc~~.sf)i.s...... 3 1 dioccoccstids (see Llioccoccstidae) rucio&hii ...... 3 1 Uioecocestinae ...... 50, 52, 53, 55, 56 ru/ic.ol/r (see C. oval(,) l)ioc~cocc~.s(us ...... 18, 20, 46, 54, 55 sp ...... 31 nc.oty1u.s...... 20, 46, 54, 55, 56 .s/)cc.s.sliii (see C. ovc~lc:) c~.spr?...... 20, 45, 46, 52, 53, 51, 56, 64, 65 .sj)ic.r~lig.(>ruTIL ...... 31, 5 1 ccrblri ...... 20 coot (see I'~ilicn) fiwiln ...... 20 copepods (Crt~stacca)...... 4, 56 . . Jtt hrnznn.n i (see I). a.spPr) Corixidac (cor~x~dbug) ...... 3, 46 novn(~gei~~~cru...... 20 Corpo[)yrzim jnrn.sc.hi ...... 8 novnrhollclndirrc~ ...... 56 C'~o1a1ca ...... 49 pnroncli ...... 20 ' . Cory~~o.somcr ...... L(3 sp ...... 20 crnolnriron ...... 26 Dioicocestidac (sce l~ioccocestidae) c.or7..s~ric.l1em...... 26, 57 1)ioicocc.slu.s (see L)io(~cocr,slu.s) .sem(,r~n.u ...... 26, 57 1)iorc.ki.c uli.s(ru ...... 24 .strztrtlo.r~rm ...... 26, 27, 57 inptcln ...... 24 .slrurtzosum, life cycle, fig ...... 27 sknrl)ilowit.srhi ...... 24 Co.srt~ocrj~hnl.u.s...... 32 "sp. P" of Stock 1985 ...... 57 dirsin.gi (see C. o1)vrlc~tzc.s) species "0"Stock ...... 24 .fi t.lollri (sec C. o/)vrlrk~~.s) species "P" Stock ...... 24 0011~le~t1e.s...... 31 sj~innter...... 24 C0lylurl.e~~~I.IZLL~.ILS ...... 14 Dipl~yllobotl~riidac...... 18, 56 I~iplzyylloOorht-iurtzdilmmurn ...... 18 Ef)o.midiostonzumuncinatum ...... 30 por1icij)edi.s ...... 18 ereynetid (see also Ereynetidae) ...... 9. 60 ucsi ...... 62 Ereynetidae ...... 34. 35 I)ij,laca.n~lhu.s(see CorzJlunriafurcijkra) Eucestoda. molecular phylogeny. relationships among major Ili/,lo/,o.sthelccwis ...... 25 groups ...... 18 Di~lostoinidae...... 13 Eucoleus contortus ...... 30 I)i/)lostow2umbr(2)i. s(!grtzmt(~turn (sce Tylodelj)lzys elongceta) Eucotyle cohni ...... 17 ccrj~sul(er t...... I? hassalli ...... 17 ~(LVI~LI~I(ofDubois & Ral~sch,1950) ...... I? nephritica ...... 18 g(4uitcna (or Guberlet, 1922) ...... 13 popowi ...... 18 nzccrgi ...... 13 Eucotylidae ...... 17 .s cheuringi ...... 13 Eupaqphium pindchi ...... 10 .sj)crlhoceum ...... 13 Eurasia ...... 60 .sl)l,crlh(rceuna /lexicaudum ...... 13 Eustronpylides elegans (see E . mergorum) .sl, alh/?ceumnzu.rmyc ~ Joyeuxilepis l~iwncinata(see 7i~triab . ) Microj)nryphium r1~Jico1li.s...... 10 ... Laemobothriidae ...... 36 shzpn7 ...... 10 1, aernobothrion ...... 61 Microphallidae ...... 16 ntrzcm (see Id. sirnile) Microsomncanlhus (scc C;onjZ,un.n'a podicipina) simile ...... 36. 60 compressus ...... 25 . . Lake Junin ...... 46 microskrjabz?zz ...... 25 Poopo ...... 46 pachy cephalus ...... 25 Titicaca ...... 46 species "TStock ...... 25 species "WStock ...... 25 elongatum ...... 8 species "Y Stock ...... 25 Pararetinometra ...... 23 species "Z" Stock ...... 25 latrrual~ccantha...... 25. 52 mites (Acari) ...... 33. 48. 59. 60 Paraschistotaenia (see Schi.stotaenia colymba) ...... 21 analgid. Sood ...... 35 Parastrigen robusta ...... 15 dcutonymph. def...... 34 Parictrruotaenia porosa ...... 23 dc~~tonymphalinscar ...... 35 Paryphostomum mdiatum ...... 10 nasal ...... 60 sp ...... 11 prclarval instar ...... 35 PatapTer bilobus ...... 11 lxctarsi ...... 35 parvisf~ino.sus (see Pelasigr pungens) ...... 11. 12. 50 protonymph. def...... 34 sp ...... 11 cl~~ill-wall...... 34. 48 . . Pebcitusfulicaeatrae ...... 5. 33. 36. 48. 60. 62 suppression of instars ...... 34 Julicaeatme <@segenae ...... 33. 36 tritonymph. def...... 34 ... Petasigm ...... 50 v~vipar~ty...... 34 australis (see also I! pungens) ...... I1 n~olecularphylogenetic studies ...... 50 caribben.sir ...... 11. 55 molluslts ...... 4 chandleri (see also P fiungens) ...... 11 rnonosto~nes(trematodes) ...... 7 coronatus ...... I I noth her blastocysts (see 'I'nlria .u mknsis) jloridus ...... 11 N(~dc?jdolrpissp . ofGallimore (1964) (see Micrasomacanthus yandivesicularis (see also i? pungens) ...... 11 rnicro.slt+bin~i) lobatus (see also I! pungens) ...... 11 lleinatodes ...... 43. 49. 50. 62 megacnnthunz ...... 11 host specificity ...... 29 neocomen.sis (see also P pungens) ...... 11 Neoboydaia ...... 60. 6 1 nitidus (see also P pungens) ...... 12. 55 coly~nbi/i)rmi...... 35 nitidus. life cycle. fig ...... 11 Neodioecocestus (see Dioecoce.stus) novemdecim ...... 12 N(!ovalif)orcr,parui.s/~ine ...... 23 oschmarini ...... 12. 55 N($/~roslo*rc.~cmrohu.stum ...... 10 pseudoneocomen.si.s ...... 12. 55 non-genetic variation (in helminths) ...... 50 pungens ...... 12. 50 ... North America ...... 60 skrjabmz ...... 12 Notocotylidae ...... 8 soochowen.si.s ...... 12 notocotylids (Notocotylidae) ...... 7 lienlsinensis ...... 12 . . No~ocolylusatten.ualu.s ...... 8 uamo.spzno.su.s ...... 12 Nyrnphulinae (Pyralidae) ...... 5 Phalacrocorax pela~r2cu.s...... 26 Ochetoccrcidae ...... 33 urile ...... 26 Ochetosomatidac ...... 17 Philophthalmidae ...... 8 Odonata ...... 3 IJhilo/)hthalmuslucipetus ...... 9 odonatc nymphs ...... 50. 51. 53. 59 Philopteridae ...... 36 Odpnlc~lhesbonariensis (Atherinidae) ...... 46 Plzi1opteru.s lzansensis ...... 37 oligocl~acteworms ...... 33 Phoenicopteridae ...... 56 Onchocercidae ...... 33 Phthiraptera ...... 33. 36 0nchorl~ynchu.s.fig ...... 27 pinnipeds ...... 57 Opisthorchidae ...... 16 Placobdella ornata ...... 34 Orchipedidae ...... 16 Plagiorchiidae ...... 17 Orclzipedu.*n lracheicola ...... 16 Ragiorchis laricol(~...... 17 Or(!.slias (Cyprinodontidae) ...... 46 maculosus ...... 17 ostracods (Crustacea) ...... 4 nohlei ...... 50 l'achylrrma paniceum ...... 16 Plegadis ...... 20 sp ...... 16 Plotnikovia podilymbae ...... 16 Pachytrelllatidae ...... 16 Podicephorus ...... 59 I'amcoenogon.imu.s ountus ...... 13 Podicephorus major ...... 39. 48. 49. 77 Par(~cunricr,ac11tnca ...... 32 Podicephorus major; bill form. fig ...... 44 lridsntnla (see I! adunca) Podiceps ...... 42. 43. 59. 60 I'nmdilepi~vsp . (sce Parajmbriaria wabsleri) auritus ...... 18. 39. 42. 48. 55. 56. 57. 60. 61. 64. 77 .u.rceus ...... 23 . . cristatus ...... 7. 40. 46. 48. 55. 57. 61. 64. 80 l'~tr(~fimbr~arr(~...... 23 jluviatilis (see Tachybr~plusrujcollis) .m.icran.lha ...... 25 gallardoi ...... 41. 43. 45. 48. 49 webslm...... 25 gallardoi. bill form. fig ...... 44 P~~mmonostornumbucepI~al(ce ...... 8 gnsegena ...... 7. 18. 20. 48. 52. 54. 55. 57. 61. 64. 78 ccceci ...... 8 grisegrna gnsegena ...... 40 88 Mrsc . PUBL. MUS . ZOOL..UNIV . MICII.. NO . 188 griseg~nc~holOoellii ...... 40 11-idenspar (see I! doli~tm) gri.seg(.na. figs ...... 19. 27 Pseitdophyllidca ...... 47. 56 I~srudo~chi~lotclenia...... 21 line ...... 61 . . zndzca ...... 21 ~ninor(see Tachy1)cef)tusnifzcolli.~) ... nigricollzs ...... 7. 18. 41. 43. 48. 52. 55. 57. (50. 61. 64. 81 ()zndc/~z~...... 21 nilymcollis cal@rnicus ...... 62 I'seur1osf)elotrema japonirum ...... 17. 48. 62 nzgticollis. figs ...... cover. 15 Pseudostm'g~a(see Sch7uartzitr~rr~ccpanduhi) occif)itelis...... 43. 46. 48. 49. 82 Psilochasmu.\ oxyurus ...... 8 occ%pilnli.sjunin. ensis ...... 41. 43 Psilostornidae ...... 8 occi/)ilnlisoccij)itc~lz.s ...... 41 hiloslor~umsp . "AS.J. Smith ...... 8 sp. "8" S.J. Smith ...... 8 occipilalis occij)italis. bill form. fig ...... 44 . . r~~bricollis(see I? grkegena) Psoroptoididae ...... 35 laczanowskii ...... 41. 43. 46. 49. 82 Ptiloxenidae ...... 35 lar;zccnowskii. bill form. lig ...... 44 Ptiloxenus ...... 60. 61. 62 Podin.l/-ss-Aechmo/)/zorusline ...... 59 colymbi ...... 35 Podicipedicoples ...... 60 mnior (see 1' mcxjor) ance ri..n.ctcnus ...... 35 muiory (see F! majol-) "Porlicijicr- nnmican.os" (see Rollandia 1-ollund) major ...... 5 60 sp...... 35 l(~ticccutla...... 25 I'~.~/Iin.u.spmir (Greater Shearwater) ...... 56 I'otlilymbus ...... 42. 43. 59 I'~]pdio/)sisgennta ...... 17 gigcls ...... 39. 56. 77 l'yralidae (Lepidoptcra) ...... 5 Renicolc pinguis ...... 16 podice/).s ...... 3. 38. 48. 50. 52. 55. 56. 59. 60. 76 . . porliceps. bill form. fig ...... 44 Reincolidac ...... 16 podiceps. ligs ...... 11 . 2 1 R~tinomelramacracnnth~os ...... 25 Poliocephal~~s...... 4 59 species "AStock ...... 25 Rhinonyssidac ...... 34. 35 R1einony~su.s...... 49. 60. 61. 62 alberti ...... 35 colymoicol(c ...... 35 arulis ...... 28 podirii(,edis ...... 35 boschanis (see I? .rninukres) podilyrnbi ...... 35 cha.smugnrclhi ...... 28 /)oliocrphali ...... 35 con.tortus ...... 28 Ribeiroia wndatr~ee...... 8 .fol.nzoszi.s ...... 28, 57 Rollandin ...... 43. 49. 59. 60. 61 line ...... 59 micr@tpra ...... 38. 46. 49 microf)terl:~.bill forni. fig ...... 44 rniwutu.~...... 28 rolland ...... 10. 37. 46. 49. 55. 57. 75 paradoxus ...... 26. 28. 57 Rusff.cnirllaclonpta ...... 32 I'onloporei(c. fig ...... 27 skrjaOzni (see R . elongl:~ta) I'orrocaecum c.rcc.aum ...... 31 we(1li ...... 32 Ryjikovilipis dubintna~...... 21 prcrelonp~rn...... 31 . . wticulalum ...... 31 dubmmac: fig ...... 51 I'oslhodiplostomum podicipitis ...... 13 Saemundssonia ...... 37 Prosthogonimidae ...... 17 murlleri ...... 37 1'rosthogonimu.s cun.eatus ...... 1 7. 5 1 Salmo gairdnc-ri (Salmonidae) ...... 46 ovakus ...... 1 7. 5 1 salmon ...... 26 Proloclej)sine (see Tlzeromyzon) Suluelinus namuycu.sh (Salmonidae) ...... 46 Protoclepsis (see Theromyzon) satellite species. def ...... 64 Sch%slocej)halus...... 56. 59 Pseudomenoj~on...... 33. 36. 61 pungilii ...... 19 dolium ...... 36 48. 60 so1idu.s ...... 19 insobns fre. scai (see P dolium) solidus. life cycle. fig ...... 19 jnni.szcmsl~.ae(see I? doliurn) Schistosomatidae ...... 7. 12 pilosum ...... 36. 60 sp...... 13 scopulncornr ...... 36 schistosoines ...... 3 shchlyi (see F! dolium) Schistotaenia ...... 5 1. 52 rolymbrr ...... 21. 53 tridens (see P (dolizcm) . . tride12.szn,.rolens (see I? dohum) 1.n dzca ...... 21 azerbaijanica (see 7: acanthorhyncha) biremis ...... 3. 22. 52. 53. 54. 55. 5'7. 59. 64 biremis major ...... 22 . . ru/i ...... 21 biremrs rnmor ...... 22 scolof,el?dm...... 21 biremis. fig ...... 51 sp . ofGallimore (1964) (see S. ,sriva.stavai) biremis. life cycle. fig ...... cover srivn.stnvai ...... 21, 53 biun.cinata ...... 22. 51. 59 . . ten~rzczrrus...... 3. 22. 47. 52. 55 clecacanthn ...... 22. 53. 54 t~nuicirr~~s.fig ...... 51 decacantha. fig...... 51 . . t~.tn~i~irr~r.s.lile cycle. fig ...... 2 1 clecacanthoides ...... 22 phylogeny ...... 58 duodecncantha ...... 22 Schizurolichus c!l(~g(ens...... 3 60 mschovi (see Schistotaenia mathwossinrtae) Scl~ronr~zitmmanig(cricu. s (see S. pendubi) Jirnbriata ...... 25 52 p(enn'u1)i...... 15 fzrnbreata. fig ...... 51 scoter (see Melwnilta) .fuhrmann.i ...... 22. 59 ... shrcw (Soricidae) ...... 52 zunzr ...... 22 Signra ...... 3. 52 jubilaea (see Schistolaenia mathruos.sia~~.ae)...... 22 coneinnu. fig-...... covcr major (see 7: hire mi.^ mcjor) . . Sltrjnbinocorrt (see Syncuarin spamnta) rnzrcza ...... 22 Slt~jnbinoclavc~decoratn ...... 32 oclacantha ...... 22 horridn ...... 32 pilatus ...... 22 ... smelt (Osmcridac) ...... 26 skyabznz ...... 22 Southro~llintc...... 26 urnlensis ...... 22 hi.s/)i(,id(L ...... 28 umlen..sis, life cycle ...... 18 specialists. def'...... 8 phylogeny ...... 52. 53. 58 Sf,ir~/ilrrice porlicil,ili.s (sce I'el(~cil~~s&licaeatrne)...... 33 Tetrabothriidae ...... 20. 47. 56 Spiruridae ...... 3 1 Tetrabothrius cf. toru1o.su.s ...... 20 SLe/)hnn.o/)i-om giSz'l(,cr-ti (see Mesor(:hisspinosus) immem'n~rs(see 1: macrocephalus) S~o~rlylotremalidae...... 17 macrocephalus ...... 20. 62 Slo.mylolrc.mngrc.bei ...... 1 7 sp ...... 20 Strc.1 )tocam cm.ssicaudn ...... 32 Tetracotyb nrdea (see SlrigeaJalconi.~) reclrc ...... 32 rIe~mmeres . Jissispim ...... 31 Striger /kl(;onis...... 7. 15 pubanovi ...... 31 ./i~lcon.i.s.lif'e cycle. fig...... 15 Tetrameridae ...... 31 Strigeidae ...... 14 Theromyzon ...... 33. 34 slro~lgylcs(Strongylida) ...... 29. 30 hiannulatum ...... 34 Synrrrnrin ciconin(...... 32 coopm...... 34 ~le(;orcltn...... 32 lineaturn (see 7: coopcri) lon..riccl.~lln...... 32 occidentalis (see 7: biannulatum) ...... 34 sp ...... 32 sexoculatum (see 7: tessulatum) S~IL(L~(LL(L...... 32 tcssulntum ...... 34 .1acl~ybcc~)tu.s...... 42. 43. 49. 59 trizonmre ...... 34 11mttinicu.s ...... 38. 43. 46. 49. 55. 56. 61. 76 Thominx (see Eucoleus contorlus) dominic.ir.s. bill form. fig ...... 44 ticks (Acari) ...... 34. 48 linc ...... 60. 61 7+c~cheof)hilusrymbiu~n ...... 8 nor~neholkcnrlircp...... 38. 75 sisowi (see 7: cymbium) pelzel?zii ...... 38 Transcoelum oculeum ...... 8 ruj?colli.s ...... 7. 29. 38. 43. 48. 50. 55. 56. 57. 59. 61. 64. 75 Trichobilharzia sp ...... 12 ru/i)lavatu.s ...... 3 76 trichostrongyloids (Trichostron~gyloidea)...... 29. 30 Erclzy [email protected]'odilymbus line ...... 59 Trichuridac ...... 29 In~nicr. (sce ConJlunriaspp.) ...... 23. 24 Tropisurus (see Tetrameres cymbiuin (see Tracheoj)hilu.s c.) U.S. National Parasitc Collection ...... 65 USSIC All Union I-Iclminihological Expeditions ...... 49 W~riolefiis(see Co@unrin spp. and llol~usilepis)...... 23. 24 Mhrrliwm (see ConJlunrin cnj~illnris)...... 23 nmnfihitricu.rn ...... 25 Jusum ...... 25 waicr boatmen (Corixidae) ...... 3 Willet (see (;(~toj)troj~horu.c) Xolalgidae ...... 35