.57

Chesapeake Science Vol. 18, No. 1, p. 34-57 March, 1977

Distribution and Ecology of Estuarine Ectoprocts: A Critical Review

JUDITH E. WINSTON' Smithsonian Institution, Fort Pierce Bureau R. F. D. 1, Box 196, Fort Pierce, Fla. 33450

ABSTRACT: While most gyiniiolacmates are restricted to waters of normal salinity, at least 3-6% are able to penetrate some distance into mixohaline water. Of this group, which includes 9 species of cyclostomes, 35 species of clenostomes, 55 species of añascan and 2J species of ascophoran cheilostomcs, the cyclostomes and the ascophorans are least tolerant of diluted salinities, the ctenostomes and the anascans are most tolerant. Like many other groups of benlhic organisms, ectoprocts show a decrease in numbers of species with decreasing salinity. Only 5 species can penetrate into waters of less than 3%o. About 20 species can be considered truly brackjsh-water organisms, being most abundant in mixohaline waters. Apparently these species possess some means of active osmoregulation, probably at the tissue level. The distribution of brackish water ectoprocts depends not on salinity alone, but also on factors of temperature, substrate availabilitj' and the general stability of the environment. Research most necessary before distribution patterns can be explained concerns the salinity tolerance of larvae and adults, lanal behavior, and physiology. Also needed are faunal studies, particularly in tropical estuarine localities.

Introduction tors as substrate, depth of water, ice cover, The special ecological and physiological Oo levels, etc. Salinity does, however, ap- features of life in brackish waters have been pear to be the major environmental factor reviewed many times (e.g. Remane and involved. Schlieper 1971; Kinne 1964, 1970; Emery, Several early studies of estuarine ecto- Stevenson and Hedgpeth 1957; Day 1951; procts concerned morphological variation in Green 1968, etc.) Estuarine and brackish waters of different salinities. Winther water areas are usually poor in species, and (1877) found variations in the stenolaemate those species living there often show adapta- Crisia ebúrnea in the Baltic area which cor- tions enabling them to cope with fluctuating related with variations in salinity. Stoliczka or stressful environmental conditions. (1869), Annandale (1907a,b, Í908, 1911, Many authors have noted that stenolae- 1915) and Robertson (1921) described sev- mate and gymnolaemate ectoprocts are usu- eral Membranipora species from Indian ally restricted to normal sea water (salinity brackish water, with delicate walls, elabo- roughly 35%D). Ryland (1970) and Remane rate development of spines and a loose con- (1971) have given figures for the number of nection to the substrate. Robertson consid- species of ectoprocts in varying salinities in ered these iBorphological features to be ef- the Baltic area from which a graphic picture fects of the low salinity environment. Lop- of the gradual impoverishment of species in pens (1903, 1905, 1906, 1907) described increasingly brackish water may be derived variations in spination in a brackish water (Fig. 1). Remane has stressed that the de- species which he called Membranipora crease in the number of species cannot be membranácea from the Netherlands, later simply correlated with salinity because the considered to be a variety of Eleclra cruslu- environments sampled vary also in such fac- lenta (Borg 1931). Important contributions to the study of ' The author has published previously under the brackish water ectoprocts of the Baltic re- name Judith E. Dudley (Ed.). gion were made by Borg (1931, 1936, 34 Distribution of Estuarine Ectoprocts 35

100 Probably the most comprehensive recent review of European brackish water species is found in Gautier's 1962 monograph. He found salinity to be a principal factor in the distribution of all cheilostomes, especially harbor-dwelling species and those character- istic of the brackish circum-Mediterranean lagoons (étangs). Gautier also noted a gen- eral improverishment of species, the occur- rence of a large number of individuals of tolerant species in brackish water localities, and a change in the composition of the fauna, with the Membraniporidae, Cellular- ina and Ctenostomata being best able to I•1•1 -2•1 -3 • ' -4- I -5•1 tolerate a slight lowering of salinity, and the Cyclostomata and the ascophoran Cheilo- DECREASING SALINITY^ stomata being more completely stenohaline. Fig. 1 . Impoverishment of ectoproct speeies in the His major contribution, however, was the Baltic Sea (after data from Remane and SchUeper description of a group of subspecies, the [1971] and Ryland [1970]), Area 1, salinity-20-30%o; area 2, salinity-10-20%»; area 3. salinity •6-10%o; Conopeum. seurati group, characteristically area 4, salinity• 3-6%»; area 5, salinity • <3%o. found in the very low salinity Mediterranean lagoons, and now shown to penetrate into 1947), who distinguished betweeti the the Pontocaspian brackish seas as well (Zev- mainly marine species Membranipora mem- ina and Kuznetsova 1965). branácea (Linnaeus), and the more truly Most of the above works pertain to the brackish water species Electra crusliilenla European coast, especially the Baltic Sea. (Pallas). In the Baltic, Borg (1931) noted No comparative study has been made of decrease in size and decreasing degree of ectoprocts recorded from mixohaline water calcification of zooids of Electra in more in all parts of the world. Except for the brackish water. above papers, the literature relating to the Hutchins (1941) studied the impact of distribution of estuarine and brackish water environmental factors, especially salinity, ectoprocts is not easily accessible to readers on growth rates, calcification, and distribu- since much of it is buried in fouling studies tion of Conopeum reticulum (now identified and confused by systematic revisions. In or- by the author as a member of the lenuissi- der to clarify the whole pattern of ectoproct mum-seurati group). Presence of lateral distribution with respect to salinity the au- spines on the zooids was dependent on a thor has attempted to gather all the informa- salinity of at least 25%o. tion on such species, from faunal lists of Osburn (1932, 1944) made a survey of estuarine regions, studies of the ectoprocts the Bryozoa of Chesapeake Bay which has of various regions of the world, and from served as a classic reference on the penetra- studies on fouling organisms, into a thor- tion of marine ectoprocts into fresh water. ough survey of their distribution. Because of Osburn described the change in the coinpo- the confusion in species identity and the sition of the ectoproct fauna from the sea diversity of the literature, a bibliography on into the estuary, with ctenostomes and the ecology and distribution of these orga- membraniporine cheilostomes being pro- nisms has been included. portionately better represented, and cyclo- stomes and ascophoran cheilostomes more Materials and Methods poorly represented in the Bay than in the Ninety-nine studies covering 56 world- sea. He also stressed that while the numbers wide localities were used in constructing the of species were reduced, the numbers of tables of estuarine species and the gradients individuals of these few species could be of brackish water penetration. Fig, 2 shows quite large at any given locality. the location of these areas with respect to 36 J. E. Winsion

KEY: H TROPICAL Hi WAR M-TEMPERATE • BOREAL-ANTIBOREAL Fig, 2. Estuarine and brackish-water ecloproct localities. 1. Gulf of St. Lawrence (Sassier and Osburn 1931; Brunei 1970). 2. Bay of Fundy (Powell and Crowell 1967). 3. Great Bay, N.H. (Winston, unpublished research). 4. Long Island Sound (Hu.'chins 1945). 5. Delaware Bay (Watts 1957; Maurer and Watling 1973). 6. Chesapeake Bay (Osburn 1944). 7. Beaufort, N.C. (Maturo 1947, 1959, 1968; Wells 1961). 8. Ponce de Leon Inlet, Daytona Beach. Fla. (Clapp and Richards 1944). 9. Mayport, Jacksonville, Harbor, Fla. (Joseph and Nichy 1955b). 10. Indian River, Fort Pierce, Fla. (Winston and Middleton [unpubl.]; Mook 1976). 11. Appalachee Bay, Fla, (Joseph and Nichy 1955a). 12. N.W. Florida (Shier 1964). 13. Texas and Louisiana Coasts (Gunter 1955; Gunter and Geier 1955; Cook 1966). 14. Tamiahua Lagoon, Veracruz, Mexico (Sandberg 1961). 15. Bay of Anlonina, Brazil (Marcus 1941). 16. Ria Deseado, Argentina (Amor and Pallares 1965). 17. Panama Harbor, Panama (Powell 197 1). 18. San Francisco Bay, Calif. (Filice 1958). 19. Admiralty Inlet, Puget Sound, Wash. (De Palma 1966). 20. Strait of Georgia, B.C. (Powell 1967; Johnson and Miller 1935). 21. New England Creek, Essex, England (Howes 1939; Cook 1960). 22. Mersey Estuary. England (Fraser 1938;Corlett 1948). 23.Tamar Estuary, and Plymouth England (Milne 1940; Mar. Biol. Assoc, U.K., 1958), 24. Baltic Sea. Kattegat Area (Borg 1930; Braltstrom 1954; Kramp 1918). 25. Baltic, including inner areas (Androsova 1952; Bock 1950; Braem 1951; Jebram 1969; Ryland 1970). 26. Western Norway (Nair 1961, 1962). 27. Norlh Sea, Riveroff Canal, Elbe Estuary. Nordostsee Canal, Schleswig-Holstein (Jebram 1969a. b; Kuhl 1972; Schutz 1963; Hag- meier 1927). 28. Former Zuiderzee, Netherlands (Vorstman 1936; Van Benthem Jutting 1922). 29. Netherlands, all areas (Lacourt 1951). 30. River D'lc and Roscoff, France (Salmon 1959; Prenant"and Teissier 1924). 31. Western Mediterranean (Gautier 1958). 32. Naples, Italy, "Lago di Palria," "Lago Fusaro" (Sacchi 1961a, b; Carrada and Sacchi 1966). 33. Adriatic-Lagoon of Venice (Neviani 1937; Gautier 1958). 34. Lagoon of Orbatello (Apolloni 1931). 35. Black Sea, Med-Azov (Lebedev 1963; Braiko I960). 36. Caspian Sea (Abrikosov 1959; Zevina 1963; Petukhova 1963; Ryland 1967; Zevina and Kuznetsova 1963). 37. Aral Sea (Abrikosov 1959), 38, Sea of Azov (Lebedev 1963; Slarostin and Permitin 1963), 39, Port Said, Egypt (Hastings 1927), 40, West Africa: vicinity of Lagos, Nigeria, and mouth of River Densu. Ghana (Cook 1 968a, b). 41 . Knysna Estuary, 5. Africa (Day, Millard and Harrison 1952). 42. Milnerlon Estuary, S. Africa (Day 1951). 43. Klein River Estuary, S. Africa (Scott, Harrison and McNae 1952). 44. Bombay Harbor, India (Karande 1968). 45. Cochjn Harbor, India (Menon and Nair 1967, 1971). 46. Madras Harbor, India (Antony Raja 1959; Daniel 1954). 47. Visapakhatnam Harbor, India (Ganapati 1958). 48. Bav of Bengal, various areas (Annandale 1907a, b, 1908, 1911 . J915; Robertson 1921). 49. Sydney Harbor area. Australia (Allen and Wood 1950; Wisely 1959; Blick and Wisely 1964). 50. Brisbane River. Moretón Bay. Australia (Straughan 1967). 51. Auckland, New Zealand (Skerman 1959). 52. Sasebo, Japan (Rucker 1969). 53. Maizuru, Japan (Rucker 1969). 54. Matsushima Bay, Japan (Toriumi 1944). 55. White Sea (Zevina 1963). 56. Kola Inlet, Murmansk Coas! (Gurjanova 1924). the littoral marine biogeographic provinces perate (22) provinces. Only 13 are found in derived by Hedgpeth (1957), The figure the tropical region. The lack of information demonstrates that most of the locations are on tropical areas makes it impossible to get in the boreal-antiboreal (21) and warm-tem- a true idea of tropical estuarine ectoproct Distribution of Estuarine Ectoprocts 37 diversity, although the locations can still be (1971, p. 5-6) adapted from the "Venice useful in obtaining some idea of the types of System" classification (Symposium in the ectoproct species found in these areas and classification of brackish waters, 1959): the factors influencing their ecology. hyperhaline = >40%o The 99 references selected from the bibli- euhaline = 30-40%o ography were used to compile Table 1•a mixohaline = <30%o list of species collected at stations with di- polyhaline = 30-18%o minished salinity. The list includes all spe- pliohaline = 18-8%o\_ cies mentioned in those references even if mesohaline miohaline = 8-3%o I they only occurred at one locality. How- oligohaline = 3-0.5%o ever, since species which occurred only once limnetic = 0.5%i could have been erroneously labelled and not truly euryhaline, only those which either Table 3 lists the estuarine and brackish occurred more than once, or occurred once water ectoprocts characteristic of the var- but in water that was definitely mixohaline ious biogeographic provinces as delimited (<30%o) in character were included in the by Hedgpeth (1957). In the case of species rest of the analysis. Wherever possible which also occur in marine environments, names have been changed to correspond the table lists only their records from the with current nomenclature. brackish water localities; their biogeo- Figs. 3, 4 and 5 summarize gradient data graphic distribution in euhaline waters may from 9 of the most complete studies on the be broader. change in composition of the ectoproct fauna with increasing brackish water pene- Results tration. Table 2 gives the salinity ranges of species BRACKISH WATER GYMNOLAEMATE collected at stations with diminished salin- SPECIES ity. Station salinities were used if available; The list (Table 1) of those species occur- otherwise, salinities were estimated from ring at least once at a station of diminished other literature on the hydrography and salinity contains 16 species of cyclostomes, physical conditions of the area. The species 52 ctenostomes, 92 añascan cheilostomes, were grouped in categories according to the and 43 ascophoran cheilostomes, or 203 salinity classification of Remane and Schlie- species in all, representing only 6% of the per (197], p. 87): (1) Stenohaline marine 3500 or so Recent ectoproct species. Those organisms or halobionts (live in euhaline species which occurred more than once or range 35-40%o to about 30%o); (2) Euryha- were definitely shown to occur in brackish line marine organisms or halobionts of the water include 9 species of cyclostomes, 35 first degree (I) •range from sea (35-40%o) species of ctenostomes, 55 species of anas- to 30-18%o salinity; (3) Euryhaline marine cans and 21 species of ascophorans, only organisms of the second degree (II) or plei- 120 species in all, or, 3% of the total Recent omesohaline organisms •range from the sea ectoproct fauna. Thus, only 3 to 6% of into water of 18-8%o; (4) Euryhaline marine gymnolaemate ectoprocts are known to organisms of the third degree (III) or mei- have penetrated into brackish water. omesohaline organisms •penetrate from Considering the number of genera in- the sea into salinities of 8-3%o; (5) Euryha- volved, it appears that there are 4 genera of line marine organisms of the fourth degree cyclostomes, 18 genera of ctenostomes, 21 (IV) or oligohaline marine organisms • genera of añascan cheilostomes and 19 gen- those which can survive in water of less than era of ascophoran cheilostomes known to 3%o. Table 2 also includes those euryhaline occur in brackish water. Bassler (1953) lists marine organisms for which brackish water 58 genera of Recent cyclostomes, 33 genera conditions appear to be optimal for survival of ctenostomes, 174 of añascan, and 207 of and reproduction or the true brackish water ascophoran cheilostomes. Therefore, about species. 7% of the total cyclostome genera (repre- The salinity categories used in this paper senting only 2 of the 5 suborders), 55% of follow those given in Remane and Schlieper the ctenostome genera, 12% of añascan 38 J. E. Winston

TABLE 1 . List of species collected at stations with diminisited salinity Species Locations Geographic Affinity Cycloslomes 1. Cris in sp. 49 Tropical 2. Crista denticulata (Lamarctc) 29 Boreal 3. Crisia ebúrnea (L.) 3,4.6,24,25.26 29 56 Boreal, Warm-temp. 4. Crisia elongala Milne-Edwards 33 Warm-temp. 5 . Crisia geniculala Smitt 56 Boreal 6. Crisidia cornuta (L.) 29 Boreal 7. Crisiella producía (Smitt) 25, 56 Boreal 8. Diaslopora flabellutn (Reuss) 33 Warm-temp. 9. Licheuopora hispida (Fleming) 25 Boreal 10. Licheuopora inlricaia (Busk) 17 Tropical 1 1. Licheuopora verrucaria (Fabricius) 4, 24, 25, 26 Warm-lemp., Boreal 12. Plagioecia palina (Lamarck) 26 Boreal 13. Tubulipora ßabellaris (Fabricius) 19, 20, 25, 26, 34 Boreal, Warm-temp. 14. Tubulipora liliácea (Pallas) 4, 25, 26, 29 Boreal, Warm-temp. 15. Tubulipora lobulaia Hassall 24, 25 Boreal 16. Tubulipora phalaiigea Couch 24, 25 Boreal Clenosfoines 1. Aeverrillia ármala (Verrill) 4, 6, 7, 12, 15 Warm-temp. 2. Aeverrillia seligera (Hincks) 4, 7, 39. 44 Warm-temp., Tropical 3. Alcyonidium choiidroidcs O'Donoghue & 41 Warm-temp. DeWatteville 4. Alcyonidium gelaiinosum (L.) 16, 24, 25, 26. 2Ç , 33 Boreal, Warm-temp. 5. Alcyonidium hauffi Marcus 7 Warm-temp. 6. Alcyonidium hirsutum (Fleming) 24, 25, 28, 29, 5t Boreal 7. Alcyonidium inamillalum Alder 7, 15, 29 Boreal, Warm-temp. 8. Alcyonidium mylili Dalyell 1,24. 30 Boreal, Warm-lemp. 9. Alcyonidium parasilicuin (Fleming) 6, 12, 25. 29 Boreal, Warm-temp. 10. Alcyonidium polyouin (Hassall) 2, 3, 4, 5. 6. 7. 12, 16, Boreal, Warm-temp. 17,23,25,26.28 ,29 ,30 11. Alcyonidium proliferans Lacourt 29 Boreal 12. Alcyonidium rhomboidale O'Donoghue 41 Warm-temp. 13. Alcyonidium veirilli Osburn 4, 5, 6, 7 Warm-temp. 14. Amaihiu sp. 13 Warm-temp. 15. Amalhia sp. 43 Tropical 16. Amalhia altérnala Laniouroux 12 Warm-lemp. 17. Amalhia cotivoluia Lainouroux 5. 6. 7, I 1, 12 Warm-temp. 18. Amalhia disions Busk 7 Warm-temp. 19. Amalhia vidovici (Heller) 4, 5, 6 Warm-temp. 20. Anguinella pálmala Van Beneden 4, 5, 6. 7, 12. 28. 29 Boreal. Warm-lemp. 21 . Arachnidium clavatum Hincks 35 Warm-temp. 22. Arachnidium fibrosum Hincks 15 Warm-lemp. 23. Bowerbankia sp. 13 Warm-temp. 24. Bowerbankia sp. ( = ß. imbrícala caspia) 38 Warm-temp. 25. Bowerbankia sp. 43 Tropical 26. Bowerbankia sp. 45 Tropical 27. Bowerbankia sp. 46 Tropical 28. Bowerbankia sp. (Indian River sp.) 10 Tropical 29. Bowerbankia gracdis Leidy 3, 4, 5, 6, 7, 12. 15, 16. Boreal, Warm-temp., Trop- 24. 25, 27, 28, 29,30. ical 32. 35, 44. 46, 47. 53 30. Bowerbankia imbrícala (Adams) 3, 16. 22, 23. 26, 29, 30, Boreal, Warm-lemp. 33 31.0. imbrícala caspia (Abrikosov) 35^ 36 Warm-temp. 32. Bowerbankia imbrícala aralensls (Abriko- 37 Warm-temp. sov) 33. Bowerbankia pustulosa (Ellis and Solander) 23, 33 Warm-temp. 34. Bulbella abscondlia Braeni 25, 27 Boreal 35. Buskla nllens Alder 25, 29 Boreal 36. Farrella repens (Farre) 28! 29 Boreal 37. Fluslrellldra hispida 1, 2,3,4, 24. 25, 26. 29, Boreal, Warm-lemp. 30, 56 Distribution of Estuarine Ecloprocts 39

TABLE 1. (Cont'd)

TABLE 1. List of species collected at stations with diminished salinity Species Locations Geographic Affinity 38. Mimosella gracilis Hincks 33 Warm-temp. 39. Nol-ella sp. 44 Tropical 40. Notelta papuensis (Busk) 44, 45 Tropical 41. Nolella gigantea (Busk) 7 Warm-temp. 42. Paludicella sp. 48 Tropical 43. Paludicella articúlala (Ehrenberg) 29 Boreal 44. Sundanella sibogae (Harmer) 7, 12, 15 Warm-temp. 45. Tanganella mulleri (Kraepelin) 25 Boreal 46. Triiicella elongata (Osburn) 4, 5, 6, 7 Warm-temp. 47. Trittcelta pedicellaia (Alder) 25 Boreal 48. Valkeria uva (L.) 24, 25, 27, 28, 29, 31 i Boreal, Warm-temp. 49. Vesicularia spinosa (L.) 29 Boreal 50. Victorella bergi (Abrikosov) 37 Warm-temp. ? 5L Victorella pavidn Saville Kent 6, 7, 24, 25, 27, 28, Boreal, Warm-temp., Tropi- 29,32,35,36,44^, 45, cal 48, 54 52. Zoobolryon veniciUatum (Delle Chiaje) 7, 12, U, 13, 31, 32, 33, Warm-temp., Trópica 1 44 CheUostomes AñASCA 1. Aelea anguina (L.) 4, 6, 7, 12, 16,40 Boreal, Warm-temp., Tropi- cal 2. Aelea ligulala Busk 16 Boreal 3. Aelea sica (Couch) 16 Boreal 4. Aetea Irutjcala (Landsborough) 25, 26 Boreal 5. Atderina arabiensis iVIenon and Nair 45 Tropical 6. Alderina smitii (Smitt) 44 Tropical 7. Amphiblestrum ßemingii (Busk) 26 Boreal 8. Amphiblestrum trifoliwn (Searles Wood) 35 Boreal 9. Antropora tiricia (Hastings) 17 Tropical 10. Aplousitia gigantea Canii and Bassler 7 Warm-temp. 11^. Aspidelecira densuense Cook 40 Tropical 12. Aspidelecira tnelolonlha (Landsborough) 27, 29, also England Boreal 13. Beania cosíala (Busk) 16 Boreal 14. Beania inermis (Busk) 16 Boreal 15. Beania iiiiermedia (Hincks) 10 Tropical 16. Beania magellanica (Busk) 16 Boreal 17. Bicellariella ciliala (L.) 23, 29 Boreal 18. Bugula sp. 8 Warm-temp. 19. Bugula sp. 9 Tropical 20. Bugula avicularia (L.) 48 Warm-temp. 21. Bugula californica Robertson 52, 53 Warm-temp.. Boreal 22. Bugula cucullata Busk 45 Tropical 23. Bugula dilrupae Busk 33 Warm-temp, 24. Bugula flabellala (Thompson) 51 Warm-temp. 25. Bugula gracilis (Busk) 4, 33 Warm-temp. 26. Bugula nerilina (L.) 7, 8, 9, 10. 11, 12, 17, Boreal (?), Warm-•tenip.. 31, 32, 33, 29, 44, 45, Tropical 49, 50, 51, 52, 53 27. Bugula pacifica Robertson 20 Boreal 28. Bugula plumosa (Pallas) 29, 33 Warm-temp. 29. Bugula spicaia (Hincks) 33 Warm-temp. 30. Bugula simplex H'mcVi 5. 8. 31 Warm-temp. 31. Bugula srolonifera Ryland 3. 7, 10. 17. 31, 32, 33 Boreal, Tropical, Warm- temp. 32. Bugula lurrila (Desor) 3, 4, 5, 6, 7, 13 Boreal, Warm-temp. 33. Callopora aurila (Hincks) 2. 3, 4. 24, 25, 35 Boreal, Warm-temp. 34. Callopora cratícula (Alder) 4, 24, 25, 26 Boreal, Warm-temp. 35. Callopora linéala (L.) 25, 26, 29, 33, 34 Boreal, Warm-temp. 36. Carbasea carbasea Ellis & Solander 24 Boreal 40 J. E, Winston

TABLE (Cont'd)

TABLE 1. List of species collected at stations with diminished sahnity Spt-cies Locations Geographic Affinity 37. Caiilibugula sp. 44 Tropical 38. Chapería patilla (Hincks) 7 Warm-temp. 39. Conopeum sp. 44 Tropical 40. Conopeum reliculum (L.) 2, 4, 15, 21. 23, 27 29, Boreal, Warm-temp. Trop- 30. 35 (?). 49, 50 ical 41. Conopeum seurali (Canu) 10, 21, 25, 27, 29, 30, Boreal, Warm-temp. Trop- 31, 32, 35(7), 36, 38 • ical 42. Conopeum lenuissimuni (Cami) 3,5,6,7,8,9(7), 10 12, Boreal. Warm-temp. Trop- 13, 40 ical 43. Conopeum rruitii Osburn 6 Warm-temp. 44. CribriUna annulata (Fabricius) 20, 24, 25, 26 Boreal 45. Crihrilina cryptooecium Norman 2 Boreal 46. CribriUna puiictata (Hassall) 2, 3, 4, 24, 25, 29 Boreal, Warm-temp. 47. CribriUna spilzbergensis (Norman) 55 Boreal 48. Cupuladria canariensis (Busk) U Tropical 49. Eleclra sp. 14 Tropical 50. Eleclra sp. 43 Tropical 5 1. Eleclra betiuia (Hincks) 10, 12, 40 Warm-temp.. Tropical 52. Eleclra bengalensis (Stolickzka) 17, 45, 48 Tropical 53. Eleclra cnislulenia (Pallas) 2, 21, 23, 24, 25, 27 28, Boreal, Warm-temp. Trop- 29, 45, 54, 55 ical? 54. Eleclra monosiachys Marcus 2,4,5,6,7,8,17,21 29 Boreal, Warm-temp. 55. (near) Eleclra monosiachys 43 Boreal 56. Eleclra pilosa (L.) 3, 4, 6, 23, 24, 25, 26, Boreal, Warm-lenip, 28, 29, 34, 35, 55 , 56 57. Eleclra I en ella (Hincks) 52, 53 Boreal, Warm-temp. 58. Eleclra verticillaia (Ellis and Solander) 26, 40 Boreal, Tropical 59. Eleclra zosiericola (Von Nordman) 35 Warm-temp. 60. Eucralea loricaia (L.) 24, 25, 29, 56 Boreal 61. Flusira foliácea (L.) 2, 24, 25, 29 Boreal 62. Membranipora sp. (nol membranácea) 6 Warm-temp. 63. Membranipora sp. (may be Conopeum len- 13 Warm-temp. uissimum) 64. Membranipora sp. (as Acanlhodesia sp.) 13 Warm-temp. 65. Membranipora sp. (äs, Acanlhodesia sp. 14 Tropical 66. Membranipora sp. 42 Boreal 67. Membranipora sp. (zi Acanlhodesia sp.) 43 Tropical 68. Membranipora sp. 46 Tropical 69. Membranipora sp. 47 Tropical 70. Membranipora arborescens (Canu and Sas- 7, 12, 17. 18 Boreal, Warm-temp., Trop- sier) ical 71. Membranipora annae Osburn 17, 40 Tropical 72. Membranipora dcvinensis (Robertson) 48 Tropical 73. Membranipora hugliensis (Robertson) 48 Tropical 74. Membranipora membranácea (L.) 22,24, 25,26,27 7, I 9 •) Boreal 75. Membranipora savarlii (Audouin) 11, 12, 13, 17. 39, 44, Warm-temp.. Trópica 45,49 76. Membranipora tenais Desor 4, 5, 6, 7, 11, 12, 29 35 Boreal. Warm-temp., Tro p- ical 77. Membranipora tuberculaia (Bosc) 5, 6, 13, 40 Warm-temp., Trópica 78. Membranipora villosa Hincks 20 Boreal 79. Membraniporella iiitida (Johnston) 25, 26, 29 Boreal 80. Menipea marionensis Busk 41 Warm-temp. 81. Parellisina curvirostris 17 Tropical 82. Scruparia ambigua D'Orbigny 16, 26, 31 Boreal, Warm-temp. 83. Scruparia chelata (L.) 31 Warm-temp. 84. Scrupocellaria sp. 51 Warm-temp. 85. Scrupocellaria beriholettii (Audouin) 31, 33, 35. 39 Warm-temp. 86. Scrupocellaria ¡olloisii (Audouin) 39 Warm-temp. Distribution of Estuarine Ectoprocts 41

TABLE J. (Cont'd)

TABLE 1. List of species collected at stations with diminished salinity Species L-ocations Geographic Affinity 87. Scrupocellaria replans (L.) 26 Boreal 88. Scrupocellaria scabra (van Beneden) 24, 29 Boreal 89. Scrupocellaria scruposa (L.) 24, 26, 29 44 (?) Boreal, Tropical (?) 90. Securiflusira securifrons (Pallas) 24, 29 Boreal 9L Tegella unicornis (Fleming) 25, 26, 29 Boreal 92. Thalamoporella golhica (var. floridana) Os.- 11. 12 Warm-temp., Tropical burn ASCOPHORA 1. Celleporaria aperia (Hincks) 39, 52, 53 Boreal, Warm-temp. 2. Celleporella hyaliua (L.) 3,4,6,7, 16 19 20 23, Boreal, Warm-temp. 24, 25, 26 3. Celleporina hassallii (Johnston) 29, 56, 26 Boreal 4. Chorizopora brogniarlii (Audouin) 34 Warm-temp. 5. Codonellina monlferrandii (Audouin) 52 Warm-temp. 6. Cryplosiila pallasiana (Moll) 2, 3, 4, 7 , 8 9, 20 23, Boreal, Warm-temp., Trop- 26, 29, 31, 32, 33 34, ical 35, 53, 50 7. Discopora lurgeuewi Ostroumoff 35 Warm-temp. 8. Escharella inmiersn (Fleming) 2, 24, 25 Boreal 9. Escharina spiuifern (Johnston) 24 Boreal JO. Euleleia evelinae Marcus 40 Tropical 11. Fenesirulina mahisii (Audouin) 34, 53 Boreal, Warm-temp. 12. Hippodiplosia sp. 3 Boreal 13. Hippodiplosia perlusa (Esper) 23, 29 Warm-temp., Boreal 14. Hippopodina feegeensis (Busk) 17 Tropical 15. Hippoporella gorgouensis (Hastings) 17 Tropical 16. Hippoporiclra janthina (Smitt) 7 Warm-temp. 17. Hippoporina americana (Verrill) 7, 40 Warm-tetnp. 18. Hippoporina verrilli Maturo and Schopf 10, 17 Tropical 19. Cleidochasma coniracnjin (Waters) 11 Tropical 20. Celleporaria mordax (Marcus) 12 Warm-temp. 21. Mamillopora sp. 44 Tropical 22. Microporella californica (Busk) 20 Boreal 23. Microporella ciliala (Pallas) 4,6, 7, 12 , 20,29 Boreal, Warm-temp. 24. Microporella umbráculo (Audouin) 17 Tropical 25. "Parasmillina trispinosa" 4, 7, 12 , ( also P uget Warm-temp., Boreal? Sound) 26. Parasinillina crosslandi (Hastings) 17 Tropical 27. Pasylhea lulipifera (Ellis and Solander) 40 Tropical 28. Rhynchozoon rostralum (Busk) 7, 17 Wann-temp., Tropical 29. Savigiiyella lafontii (Audouin) 39. 45 Warm-temp., Tropical 30. Schismopora americana (Osburn) 4 Warm-temp. 31. Schiiobrachiella sanguínea (Norman) 33 Warm-temp. 32. Schizomavella auriculala (Hassall) 35 Warm-temp. 33. Schizomavella linearis (Hassall) 29, 35. 45 Boreal, Warm-temp., Trop- ical 34. Schizoporella sp. 35 Warm-temp. 35. Schizoporella sp. 44 Tropical 36. Schizoporella biaperia (Michelin) 4 Warm-temp. 37. Schizoporella cornula (Gabb and Horn) 7 Warm-temp. 38. Schizoporella errata (Waters) 3. 4, 6. 7, 31. 33 Boreal, Warm-temp. 39. Schizoporella unicornis (Johnston) 8, 9, 10, U, 12, 20, 30, Boreal, Warm-temp., Trop- 39, 43, 52 ical 40. Smilloidea prolifica Osburn 52,53 Boreal, Warm-temp. 41. Umbonula verrucosa (Esper) 33 Warm-temp. 42. Viiialicella ubérrima Harmer 40 Tropical 43. Watersipora subovoidea (D'Orbigny) 10,31,40, 45, 49, 52, 53 Boreal, Warm-temp.. Trop- ical 42 J. E. Winston

100- BAY OF FUNDY * CHANGES JN COMPOSITION OF ECTOPROCT 80 FAUNA IN BRACKISH WATER < § 60 A few of the references used were com- plete enough to allow interpretation of 40- O- 20 a ^^.^i^CX. D- """^^^ ^^^*^=^ CHESAPEAKE BAY cF ::« -Í* REGION i III

REGION I

REGION I B 100-1 BEAUFORT, N.C, < 80 3 < 60

O 40

^ 20-

0- -^Ö- REGION I II III

N.W. FLORIDA DECREASING SALINITY Fig. 3. Changes in composition of ectoprocl faunas from marme to brackish water in boreal localities. (A) Bay of Fundy. N.S.: i, outer Bay stations; ii, inner Bay stations; iii. brackish-water stations (based on data in Powell and Crowell 1967). (B) Long Island Sound: i. localities with salinities above 28%o; ii. localities with salinities 20-28%»; ¡ii. typical oyster ground species; iv, inner harbor species (based on data in Hutchins 1 945). (C) Baltic Sea: i. western Norway (marine); ii. Baltic transitional zone; iii, s.w. part of the Sea; iv, central REGION I pan of the Sea (with bays); v, river mouths (based on data in Bock 1950; Androsova 1962; Jebram 1969a, 1969b). Data given as percent of total ectoproct fauna DECREASING SALINITY each group comprises in each region: open squares, Fig. 4. Changes in composition of ectoproct faunas ctenostomes; stars, añascan cheilostomes; open circles, from marine to brackish water in North American ascophoran cheilostomes; starred circles, cyclostomes. warm-temperate localities. (A) Chesapeake Bay-At- lantic Shelf: i. Atlantic Shelf (marine); ii. Bay localities with salinity greater than 18%o; iii. Bay localities with cheilostome genera, and 9% of ascophoran salinity J0-]8%o; iv. Bay localities with salinity less cheilostome genera have been found in than I0%o (based on data in Osburn 1944; Maturo 1968). (B) Estuarine-offshore localities, Beaufort, brackish water. Cyclostomes and asco- N.C: i. offshore (marine); it, esluartne-sound; iii, estu- phoran cheilostomes appear least tolerant of arine (based on data in Maturo 1957, 1959, 1968). (C) diluted salinities, while añascaos (mainly N.W. Florida: i. Gulf of ivie.xico (marine); it, marginal membraniporine forms) are somewhat more stations; iii, brackish stations (based on data in Shier tolerant, and ctenostomes contain a major- 1964). Data given as percent of total ectoproct fauna each group comprises in each region: open squares, ity of genera able to survive at least some ctenostomes; stars, añascan cheilostomes; open circles, dilution of salinity. ascophoran cheilostomes, starred circles, cyclostomes. Distribution of Estuarine Ectoprocts 43

00-1 PLYMOUTH, ENGLAND localities with respect to salinity, the gra- dients still are useful in deterinining general 80 - patterns. 60- Fig. 3 shows gradient patterns for 3 bo- 40- real areas: (A) the Bay of Fundy, (B) Long 2::^---»-•^ Island Sound, and (C) the Baltic Sea. Fig. 4 o 20- o---^^~¡e<^ illustrates patterns for North American # n "- ^^^o warm-temperate localities: (A) Chesapeake REGION I 11 III Bay, (B) Beaufort, N,C., and (C) North- west Florida. Fig. 5A shows the pattern for B 100-1 MED - PONTOCASPIAN SEAS Plymouth, England (warm-temperate), while 53 shows the change in composition of the ectoproct fauna from the Mediterra- <3 nean (Adriatic) to the Pontocaspian region. Patterns for a tropical region (India) are shown by Fig. 5C.

REGION I SALINITY TOLERANCES OF ECTOPROCT SPECIES c 00-, INDIA-COCHIN HBR. < 80 - Table 2 summarizes the literature on sa- < linity tolerances of various ectoproct species 60 - occurring in brackish water. The largest 40^ S>-- _-

TABLE 2. Salinity ran es of species collected at stations willi diminished salinity. I. Remane's "Eurylialine marine organisms of the first degree found in euhaline and polyhaline regions. To 18%o. Cycloslomes 18. Electra monostachys J. Crisia ebiiniea' 19. Electra lenella 2. Crisiella producía' 20. Eleclra verlicillala 3. Lichenopora hispida' 21 Eue ratea loricala' 4. Lichenopora iiuricain 22 Fluslra foliácea' 5. Lichenopora verrucaria' 23. Membranipora annae 6. Tubulipora flabellaris' 24. Membranipora arborescens 7. Tubulipora lilicjcea ' 25. Membranipora savartii 8. Tubulipora lobulala' 26. Membranipora tuberculata 9. Tubulipora phalangea' 27. Membraniporella nilida' Cienoslomes 28. Parellisina curvirostris 1. Aeverrillia seligem 29. Scruparia ambigua 2. Alcyoiiidium mainillatuin' 30. Scrupocellaria bertholettii 3. Alcyouidium mytili 31. Scrupocellaria scabra ' 4. Alcyouidium parasilicurn 32. Scrupocellaria scruposa' 5. Amathia convohila 3 3. Securiflustra securifrons ' 6. Arachnidium clavaium 34. Thalainoporella gothica var. ßoridana 7. Arachnidium fibrosum'- Ascophorans 8. Bowerbankia sp. (Indian River sp.) 1. Celleporaria apena 9. Nolelln papuensis 2. Celleporina hassallii 10. Sundanella sibogae- 3. Discopora lurgenewi 1 ) . Zoobolryon verlicillaluni 4. Escharella iinmersa' Anascans Escharina spinifera' 1. Aelea anguina Fenesirulina ntalusii 2. Amphibiestrum Irifolium Hippopodina feegeensis 3. Aniropora linda Hippodiptosia perlusa- 4. ßicellariella ciJiala ' • - Hippoporella gorgonensis 5. Bugula avicularia- 10. Hippoporina verrilli 6. Bugula cali fornica 11. Microporella ciliata 7. Bugula gracilis 12. Microporella umbracula 8. Bugula neriiina 13. Parasmiilina crosslandi 9. Bugula plumoscr 14. Parasminina irispinosa J 0. Bugula simplex 15. Pasylhea tulipifera I 1. Bugula slolonifera 16. Phynchozoon roslratum 1 2. Bugula lurrila 17. Savignyella lafonlii 13. Callopora cratícula' 18. Schizomavella auriculaia 14. Callopora linéala' 19. Schizomavella linearis 15. CribrUina annutaia' 20. Schizoporella unicornis 16. CribrUina punclata' 21. Srnilioidea prolifica 17. Eleclra bellula 22. Watersipora subovoidea U. "Euryhaline marine animals of the second degree;" occur from the sea into the pleiomesohaline zone 1 8-8%o (Pleiomesohaline marine organisms). Cyclosfomcs Anascans iNone 1. Aetea trúncala 2. Aspidelecira densuense'- Ctenostomcs 3. Aspidelecira inelolontha'- 1. Alcyonidium gelalinosum 4. Callopora aurila 2. Alcyonidium hirsuliim 5. Carbasea carbasea 3. Alcyonidium parasilicuni 6. Conopeuni truiiti 4. Alcyonidium polyouin 7. Electra bengalensis- 5. Alcyonidium verrilli 8. Electra pilosa 6. Amathia vidovici 9. Eleclra zosiericola 7. Anguinella palinata 10. Membranipora devinensis- 8. Bon'crbankia imbricata I 1. Membranipora hugliensis 9. Buskia nilens 12. Membranipora membranácea 10. Fur relia repens 13, Tegella unicornis 1 1. Fluslrellidra hispida Ascophorans I 2. Triticella elongata 1. Celleporella hyalina 13. Triticella pedicellala 2. Cryplosula pallasiana I 4. Valkeria uva 3. Schizoporella errata Distribution of Estuarine Ectoprocts 45

TABLE 2. (Cont'd) III. "Euryhaline marine organisms of the third degree;" occur from the sea to S-S'/oo (iVIeiomesohaline marine organisms). Cycloslomes Anascans None 1. Coiwpeum reliculum 2. Conopeum seuraii C(eiios(omes 3. Conopeum lenuissimum 1 Bowerbankia gracilis 4. Electra cnislutenia 2 Bowerbankia imbiicala caspia 5. Mernbranipora sp, [Ches. Bay sp.] 3 Bowerbankia imbricóla aralensis 6. Mernbranipora leniiis 4, Bulbella abscondila Ascophorans 5. Tanganella muHeri- None JV. "Euryhaline marine organisms of the fourth degree: " to < S^/oo (Oligohaline marine organisms). Cycloslomes Anascans None 1. Conopeum seuraii Clenosloines 2. Elecira crustulenla 1 . Viclorelta bergi'^ 2, Victorella pavida Ascophorans 3. Paludicella arlicutala None Of the above species the following may be considered true brackish water species according to the definition of Remane and Schlieper (1971), "Brackish w ater species are those which abound in brackish water and occur only occasionally in the sea or in fresh water Cycloslomes 2. Aspideleclra densuense'- None 3. Conopeum reliculum Ctenoslomes 4. Conopeum seuraii TridceHa elongata 5. Conopeum lenuissimum Bowerbankia gracdis 6. Conopeum Iruilli Bowerbankia imbrícala caspia 7. Electra cruslulenia Bowerbankia imbrícala aralensis 8. Elecira zoslericola Bulbella abscondila 9. Memhraniporn deviensis Tanganella mullerl 10. Mernbranipora hugliensis Victorella bergi 1 1. Mernbranipora sp. (Ches. Bay sp.) Viclorella pavida 12. Mernbranipora tennis Anascans Ascophorans 1. Aspideleclra melolontha 1. Crypiosula pallasiana (possibly) ' May occur at a lower salinity in Baltic. - No salinity given at any locations, estimated position.

BRACKISH WATER BIOGEOGRAPHY OF Discussion ECTOPROCTS DISTRIBUTION OF ECTOPROCTS IN In Table 3 the species occurring in brack- BRACKISH WATER ish water are grouped according to the bio- geographic regions (boreal-antiboreai, Gradient patterns warm-temperate and tropical) in which they Distribution patterns for the boreal re- occur. Seventy-four species are characteris- gion are best illustrated by the data from the tic of the boreal-antiboreai region, including Bay of Fundy (Fig. 3A) and the Baltic Sea 8 cyclostomes, 17 ctenostomes, 34 anascans (Fig. 3C). The number of cyclostomes and 15 ascophorans. Seventy-seven species shows a slight increase into the upper poly- are found in the warm-temperate region: 4 haline zone, but then decreases rapidly to 0. cyclostomes, 25 ctenostomes. 32 anascans The number of ctenostomes shows a percent and 16 ascophorans. In the tropical region increase from euhaline into mixohaline wa- there are 41 species: 1 species of ctenos- ter, then decreases to 0. Ascophorans make tome, 22 species of anascans and 11 species up a large percentage of the ectoproct spe- of ascophoran cheilostomes recorded. cies of the euhaline zone, then show a grad- 46 J. E. Winston

TABLE 3. Estuarine and brackish water ectoprocts characteristic of various biogeographic regions. I. Boreal and Antiboreal Regions 11. Callopora aurita Cydosloines 12. Callopora cratícula 1. Crisia ebúrnea 13. Callopora linéala 2. Crisiella producta 14. Carbasea carbasea 3. Lichenopora hispida 15. Conopeum reliciJum 4. Lichenopora verrucaria 16. Conopeum seurali 5. Tubulipora flabellaris 17. Conopeum lenuissimum 6. Tubulipora liliácea 18. Cribrilina annulata 1. Tubulipora lobulaia 19. Cribrilina punctala h- 8. Tubulipora phalangea 20. Eleclra cruslulenia Ctcnostomes 21. Eleclra monostachys 1. Alcyonidium gelaliriosurn 22. Eleclra pilosa 2. Alcyonidium hirsulum 23. Eleclra lenella 3. Alcyonidium mamillalum 24. Eucralea loricaia 4. Alcyorddium myiili 25. Flustra foliácea 5. Alcyonidium parasilicum 26. Membranipora arborescens 5. Alcyonidium polyourn 27. Membranipora membranácea 7. Anguinella pálmala 28. Membranipora tenais 8. Bowerbankia gracilis 29. Membraniporella nilida 9. Bowerbankia imbrícala 30. Scruparia ambigua 10. Bulbella abscondita 31. Scrupocellaria scruposa 1 (. Buskia nilens 32. Securiflustra securifrons 12. Farrella repens 33. Tegella unicornis 13. Fluslrellidra hispida Ascophoran Cheiloslomcs 14. Paludicella articúlala 1. Celleporaria apena 1 5. Tanganella mulleri 2. Celleporella hyalina 16. Trilicella pedicellata 3. Celleporina hassallii 17. Victorella pc.vida 4. Cryplosula pallasiana Anascan Cheilostomes 5. Escharella immersa 1. Aetea anguina 6. Escharina spinifera 2. Aetea trúncala 1. Feneslrulina malusii 3. Amphibleslrum Irifolium 8. Hippodiplosia perlusa 4. Aspidelecira meloloniha 9. Microporella ciliaia 5. Bicellariella ciliaia 10. Parasmiitina trispinosa(?) 6. Bugula avicuiaria 11. Schizomavella linearis 1. Bugula call fornica 12. Schizoporella errata 8. Bugula nerilina(?) 13. Schizoporella unicornis 9. Bugida slolonifera 14. Smitioidea proliflca 10. Bugula turrila 15. Watersipora subovoidea

U. Warm Temperate Region n. B. imbrícala aralensis(?) Cyclcslonies 18. Bowerbankia sp. (Indian River sp.) 1. Crisia ebúrnea 19. Bowerbankia pustulosa 2. Lichenopora verrucaria 20. Fluslrellidra hispida 3. Tubulipora flabellaris 2 1. Sundanella sibogae 4. Tubulipora liliácea 22. Trilicella elongata Ctenoslomes 23. Viciorella bergi(?) 1. Aeverrillia armata 24. Viciorella pavida 2. Aeverrillia setigera 25. Zooboiryott verlicillatum 3. Alcyonidium gelatinosum Anascan Cheilostomes 4. Alcyonidium mamillatunt 1. Aeiea anguina 5. Alcyonidium inylili 2. Beania intermedia 6. Alcyonidium parasilicum 3. Bugula avicuiaria 7. Alcyonidium polyoum 4. Bugula californica 8. Alcyonidium verrilli 5. Bugula gracilis 9. Amalhia convolula 6. Bugula neritina 10. Amalhia vidovici 7. Bugula plumosa 11. Anguinella pálmala 8. Bugula simplex 12. Arachnidiuin clavatum 9. Bugula slolonifera 13. Arachnidium fibrosum 10. Bugula lurrita 14. Bowerbankia gracilis IJ. Callopora aurita 15. Bowerbankia imbrícala 1 2. Callopora cratícula 16. Bowerbankia imbrícala caspia 13. Callopora linéala Distribution of Estuarine Ectoprocts 47

TABLE 3. (Cont'd) 14. Conopeum reliculum 32. Thalarnoporella golhica 15. Conopeum seuraii Ascophoran Cheiloslomes 16. Conopeum tenuissimum 1. Celleporaria apena \ 7. Conopeum Iruitii 2. Celleporella hyalina 18. Cribrilina punclata 3. Cryptosula pallasiana 19. Electra bellula 4. Discopora lurgenewi 20. Eleclra crusiulenia 5. Feneslrulina nialusii 21. Eleclra monoslachys 6. Hippodiplosia perlusa 22. Eleclra pilosa 1. ¡iippoporina verrilli 23. Eleclra lenella 8. Microporella ciliala 24. Eleclra loslericola 9. Parasmiirina irispinosa 25. Mernbranipora [Ches. Bay sp. 10. Savignyella lafonlii 26. Mernbranipora arborescens 1 I . Schizoinavella auriculala 27. Mernbranipora savarlii 12. Schizoniavella linearis 28. Mernbranipora lenuis 13. Schizoporella errala 29. Mernbranipora luberculala 14. Schizoporella unicomis 30. Scruparia ambigua 15. Smilloidea prolifica 3 1. Scrupocellaria bertholellii 16. Walersipora subovoidea

III. Tropical Region 12. Eleclra veriicillala Cyclostomes 13. Mernbranipora annae I. Lichenopora inlricala 14. Mernbranipora arborescens Ctenoslomes 1.5. Mernbranipora devinensis 1. Aeverrillia seligera 16. Mernbranipora hugliensis 2. Amaihia convolula 17. Mernbranipora savarlii 3. Bowerbankia gracilis 18. Mernbranipora lenuis 4. Bowerbankia sp. (Indian River sp.) 19. Parellisina curvirosiris 5. Nolella papuensis 20. Scrupocellaria scruposa(?) 6. Viclorella pavida 21. Thalarnoporella golhica 7. Zoobotryon veriiciUalum Anascan Cheiloslomes Ascophoran Cheiloslomes 1. Aniropora tincia 1. Cryplosula pallasiana 2. Beania intermedia 2. Hippopodina feegeensis 3. Bugula neriiina 3. Hipporina verrilli 4. Bugula slolonifera 4. Hipporella gorgonensis 5. Conopeum reliculum 5. Microporella umbráculo 6. Conopeum seuraii 6. Parasmittina crosslandi 7. Conopeum lenuissimum 7. Rhynchozoon roslralum 8. Eleclra bellula 8. Savignyella lafonlii 9. Eleclra bengalensis 9. Schizoinavella linearis 10. Eleclra crusiulenla(?) 10. Schizoporella unicornia 1 1. Eleclra monoslachys 1 1. Walersipora subovoidea ual decrease to 0. Membraniporine anas- have in the same manner as in boreal re- cans share dominance with ascophorans in gions, increasing slightly in species number, euhaline water, but as the salinity becomes then decreasing rapidly. Ascophorans also increasingly dilute, their share of the popu- show the same rapid decrease in percent of lation rises, until at the most brackish sta- fauna, but ctenostomes become increasingly tions one species of añascan usually makes important in the polyhaline and raesohaline up 100% of the ectoproct fauna. regions and remain even in the oligohaline Although Long Island Sound falls into the region. Anascans remain important. Con- northern end of the warm temperate zone tinuing down the Atlantic coast, the pattern biogeographically, the distribution of the ec- for Beaufort, N.C. (Fig. 4B) is similar to toproct fauna appears more characteristic of that for Chesapeake Bay, though cyclo- the boreal pattern, so it has been included in stomes decrease more sharply and ascopho- the boreal category (Fig. 3B). rans show less of a decline. In the north- Faunal gradients for the warm-temperate west Florida region (Fig. 4C) the pattern for waters of the Chesapeake Bay area (Fig. cyclostomes and ascophorans stays the same, 4A) show that cyclostomes appear to be- but that for anaseans and ctenostomes is 48 J. E. Winston somewhat different. Ctenostomes increase bers of species of the other groups repre- into the lowest salinity location surveyed, sents a true ecological limitation or is merely which however, is probably still in the poly- an effect of lack of sampling. haline zone, and anascans appear to decline somewhat. FACTORS INFLUENCING DISTRIBUTION The pattern for the Plymouth, England Salinity area (Fig. 5A) in general seems similar to Poor tolerance of reduced salinity is ap- that for N.W. Florida, though numbers of parently the chief factor responsible for the cyclostoraes decrease less abruptly. distributions reported above, with cyclos- Fig. 5B shows the change in composition tomes and ascophoran cheilostomes being of the ectoproct fauna from the Mediterra- least tolerant and membraniporine añascan nean (Adriatic) to the Pontocaspian region. cheilostomes and ctenostomes most toler- While the climate in this area may be more ant. These differences in tolerance may be extreme, the pattern from the Mediterra- related to differences in morphology and nean through the Black Sea to the Caspian physiology between the groups. Sea fits that for the other warm-temperate Ectoprocts, with their microscopic body areas, with ctenostome proportions rising size, have no excretory systems (Hyman above those of the anascans, while the num- 1959), and presumably, any active osmo- ber of cyclostomes declines rapidly. Asco- regulation (homiosmotic behavior) must be phorans appear to decline abruptly also, carried out by the body surfaces (body wall, though Black Sea populations of Cryptosula tentacles, etc.). According to Schlieper pallasiana can survive salinities as low as (1971) those organisms which show only a 12''/oo. In this gradient the salinity not only slight degree of euryhalinity (probably those decreases, but the composition of the salt which do not penetrate beyond the polyha- content changes (especially in the Caspian line region) generally are passively poikilos- and Aral Seas), perhaps also affecting the motic (their internal salt concentration will distribution pattern. passively adjust to the concentration of the Data on changes of composition of ecto- external medium). The truly brackish water proct faunas in a tropical area (Fig. 5C) also species (those which can live in water of low indicate the decrease in abundance of cy- salinity without reductions of size or loss of clostomes and ascophorans and the joint activity) are homiosmotic. dominance of ctenostomes and anascans at Cyclostome morphology may help to ex- the lowest salinities encountered. plain their poor tolerance of lowered salini- Biogeography ties. The zooids are long and tubular with a rigidly calcified wall which prevents expan- From Table 3 it appears that cyclostomes sion with increasing volume when the salin- are more diverse in brackish waters of the ity of the external medium is reduced. On boreal region, while higher numbers of spe- the other hand, the terminal membrane cies of ctenostomes are known in the warm- which closes the distal end of the zooid, may temperate region. It is not known if this be more permeable than the operculum change in composition is just characteristic closing the orifice of cheilostomes, thus of the estuarine fauna, or if it occurs in the making it impossible for them to escape euhaline region as well. The ratios of anas- short term salinity fluctuations (such as cans and ascophorans show no important those found in harbors) merely by closing up differences between the two regions. Be- tightly as a mussel or an ascophoran cheilos- cause of the limited amount of information tome might. Crista ebúrnea (reported from available on ectoproct faunas of tropical 8 localities) appears to be the most euryha- brackish water it is difficult to make any line cyclostome. statements about the distribution of the dif- The ascophorans are second poorest in tol- ferent groups compared to boreal and erance of brackish water. While an asco- warm-temperate regions. The lack of cyclos- phoran, with its calcified wall structure and tomes is apparently real; it is difficult to calcareous operculum has some protection ascertain whether the more restricted num- from the short terra fluctuations that might Distribution of Estuarine Ectoprocts 49 occur in harbors or estuary mouths, their ity was about 35%o, Marcus (1926) sub- strong calcification apparently prohibits jected them by gradual stages to increased most of them from making the changes in and decreased salinities. The reactions of volume, and perhaps the regulation of vol- the zooids to reduced salinity were indicated ume that would permit them to survive by reduced response to mechanical stimula- brackish water conditions. Only 3 ascophor- tion of the tentacles. Farrella repens first ans (Table 2) occur in water of the pleiome- showed reduction of sensitivity at 28%o; and sohaline region (18-8%o); Schizoporella er- at 21%o the tentacles which at first showed rata, Cryplosula pallasiana and Celleporella no response to mechanical stimulation, be- hyalma. It should be noted that of these, came adapted to that salinity and regained Celleporella has a simple primary wall (holo- their irritability within one hour. Electra pi- cyst) uncovered by any secondary thicken- losa appeared to be less tolerant of salinity ing (Ryland 1970). The other two species reduction, with most zooids of the Electra possess the type of secondary calcification colonies being able to adapt to 20%o, but known as a tremocyst in which the pseudo- dying at 17.5%o. pores (plugs of tissue from the underlying The reactions of these two species ap- cell layers whose epithelium spreads over proach those described for many euryhaline the primary wall to lay down the secondary organisms. The body volume first increases layer) cover the frontal surface in a more or more or less markedly (indicated by insensi- less regular manner (Ryland 1970). It may tivity of the tentacles), then the volume be that this regular distribution of tissue slowly returns to its original level, and the plugs makes it easier for the zooid to sustain individuals are able to move normally (e.g., volume changes. the return to irritability of the tentacles) Like the ascophorans the weakly euryha- with no or only slight injury. In many cases, line anascans appear to be poikilosmotic, this kind of volume regulation has been perhaps functioning in the same manner as shown to be an active process. the mussel Mylilus edulis, in which internal Still greater adaptability is shown by a and external salt concentrations are the truly brackish water species such as Cono- same, and in brackish water, ciliary activity, peuin tenuissimum. Experimental work car- size, and activity of shell-producing tissue ried out by the author showed that zooids (especially CaCO., secretion) are reduced were capable of adapting to a drop in salin- (Schlieper 1971). When environmental con- ity more rapid than they would be likely to ditions become too stressful the organism experience in nature. Colonies which had closes up to await their amelioration. This been maintained in the laboratory for sev- type of behavior would seem to explain the eral weeks at 15-16%o were placed in 8%o occurrence of the euryhaline harbor species filtered seawater. A few polypides ex- discussed by Gautier (1962), which in- panded immediately and then quickly re- cluded some cellularine anascans (e.g., Bug- tracted. Thirteen minutes later polypides ula spp), ctenostomes and a few ascophor- expanded again and were able to move their ans, living in environments which were char- tentacles, but ciliary activity had slowed so acterized by sudden, sharp, but short-term that the waves could clearly be seen. Within variations in salinity and temperature. Ac- 22 minutes other polypides had emerged, cording to Gautier, these shallow water spe- but tentacles looked misshapen and bent, cies (often important as fouling organisms) especially near their free ends (apparently can survive short duration variations in sa- the "Ekelstellung" or "attitude of aversion" linity of not greater than 10%o, and can live described by Marcus |1926] for the tenta- at least temporarily in waters where the sa- cles of Farrella repens when the salinity linity is in the range of 28%o. change was too drastic). In 47 minutes time The membraniporine cheilostome Electra the expanded polypides began to look more pilosa, and the carnose ctenostome Farrella nearly normal. Tentacles were still bent, but repens probably fall into a more euryhaline were no longer twisted. After 60 minutes, category. Using specimens of those species most polypides appeared normal, and when collected on the North Sea where the salin- observed 90 minutes later, the ciliary activ- 50 J. E. Winston ity had increased again so that it was no in an area like Chesapeake Bay; however, in longer possible to see the waves dearly. the Cochin area with its dramatic environ- Measurements made on 6 polypides of one mental changes during the year, physiologi- colony before and after the salinity drop cal races would appear to replace each other showed no significant difference in tentacle in time rather than in space. width, tentacle length, zooid width, lophop- hore diameter, or mouth diameter, indicat- ing that the original volume had been re- Temperature gained. The colonies were followed for a Next to salinity, temperature is probably week thereafter while being maintained at the most important factor influencing the the low salinity, without noting any degen- distribution of estuarine ectoprocts. As eration of the polypides. Gautier (1962) points out, on a local scale, The greatest tolerance to lowered salini- temperature controls the life cycle of ecto- ties is shown by the ctenostomes, a group procts. The spring rise in temperature stim- lacking in calcification of the body wall. This ulates the development of phytoplankton feature apparently gives the zooids the flexi- and thereby initiates simultaneously a proc- bility to adapt to widely varying osmotic ess of active budding. In various degrees of conditions. Victorella pavida is one of the intensity according to the species it also most euryhatine of the brackish water stimulates sexual reproduction. Ryland forms, having been collected in salinities (1970) noted that temperature is especially ranging from fresh water to 28-30%o. In important in the bathymétrie distribution of Chesapeake Bay Osburn (1944) found it ectoprocts in the Norwegian fjords, shallow occurring between 3 and 27''/oo, but growing water species seeming to require a high sum- best between 10 and 12%o. In Cochin Har- mer temperature for breeding, while deeper bor, India, a tropical estuary where the wa- water species either do not need or cannot ter ranges from euhaline salinities in the survive the higher summer temperature premonsoon period to almost fresh during and/or the cold of the surface water in win- the monsoon, Menon and Nair (1967a and ter. Since estuarine and brackish water situ- b, 1971) found Victorella pavida colonies ations are usually characterized by both apparently adapted to the ambient salinities warmer (summer) and colder (winter) tem- at the time they settle and grow. Specimens peratures (Emery, Stevenson, Hedgpeth collected at the same locality during the low 1957), this is certain to affect the distribu- salinity period (September) and the medium tion of many ectoproct species. salinity period (December) had different Cyclostomes apparently are the most optimal and lethal limits. The specimens stenothermal as well as stenhaline of the collected in September were all able to sur- living orders of ectoprocts, and many spe- vive in salinities of 0, 2, and 5%o, while cies appear to prefer cold water to warm. tolerance decreased with increasing salinity This may be another reason why the number until only 5% could survive 30%o. However, of cyclostomes decreases so rapidly in estua- the specimens collected in December could rine areas. It may also help explain why the not survive fresh water for 24 hours; 22% slight increase in percentage of cyclostomes survived 32%o, and their optimal salinity lay found in the polyhaline zone in boreal areas between 16 and 24%o. does not occur in warm-temperate areas. Carrada and Sacchi (1964) found that ia- Among the ctenostomes one group in par- goonal (Lago Fusaro, Naples, Italy) popula- ticular•the suborder Carnosa •may be tions of Victorella pavida occurring in differ- more sensitive either to temperature or to ent environmental situations formed a chain the combination of high temperature and of physiological subpopulations, each decreased salinity. This group is very com- adapted to certain conditions ranging from mon in polyhaline and meiomesohaline fresh water to almost fully marine condi- brackish water of boreal areas, occurs in tions. This type of physiological differentia- warm-temperate brackish water areas, but is tion in space may explain the occurrence of increasingly replaced by members of the Victorella pavida under different conditions other groups of ctenostomes, and does not Distribution of Estuarine Ectoprocts 51 seem to have been recorded from brackish covered bottoms generally support diverse water in the tropical region. ectoproct populations in coastal areas, but Seasonal rhythms in ectoproct life cycles this biotope seldom occurs in brackish water may help them tolerate extreme tempera- except near river mouths. Day (195 L) has ture conditions. For example, Carrada, Sac- summarized the importance of substrate in chi, and RigiUo (1966) studied the life cy- estuarine areas: cles of extoprocts living in a littoral lagoon There is no doubt that the substratum has a to the west of Naples, Italy. They found the very profound effect on the constitution of the life cycles of the species occurring there, fauna and the distribution of the component particularly Victorella pavida and Bower- species. Rocky areas are commonest at the bankia gracilis, to be closely attuned to the mouth, and rock-loving species are largely lim- seasonal variations. In spring, when envi- ited to this section of an estuary, although they ronmental conditions are relatively mild (O, will also occur on the poles of bridges and high, salinity relatively low, temperature wharves, buoys and in tropical countries on the mild) rapid asexual growth and develop- roots and trunks of mangroves. . . . But even ment occur, while in summer, when the con- in these situations the fauna is scanty, possibly ditions are much more rigorous than those because ... the surfaces are covered with a found in the sea (high temperature and lack thin film of mud .... The richest parts of the estuary are the banks of muddy sand, particu- of O;. in places) sexual reproduction occurs, larly those overgrown by Zoslera which pro- allowing adaptation to unfavorable condi- vides shelter for small surface forms. . . . tions by means of planktonic larvae which can settle elsewhere; populations are re- The euryhaline species which preferred duced, or special resistant stages, e.g., the rocky areas in the coastal region generally hiburnaeula of Victorella pavida, are pro- make a transition to the phytal zone: brack- duced. In the fall when environmental con- ish water algae, and aquatic flowering ditions again become mild, the populations plants, Ruppia, Zostera, Potamogetón, etc. recover and grow until partially blocked by (Remane 1971). In addition some species low winter temperatures. from hard substrates start to live epizooi- Physiologically the importance of temper- cally on other organisms to a great extent, ature to brackish water animals can be ex- e.g., Alcyonidium polyoum in the Baltic plained by its effect on osmoregulation. The lives on the gastropods Liltorina and Zip- permeability of living membranes generally pora (Remane 1971), and, in San Francisco increases with increasing temperature, and Bay lives on Nassarius obsoletas (Filice as Schlieper (1971) states, "Apparently not 1958). all temperate brackish water species are able to perform the required higher osmo- Larval Distribution regulatory work in brackish vv'ater of a low Hutchins (1941) has pointed out the im- salinity and at a higher temperature." This portance of the larva in determining survival factor may explain why some of the less of estuarine ectoprocts. During transplanta- euryhaline species are unable to survive in tion experiments with one species of ecto- brackish water, or are only present during proct he found that adults of other species the colder months, or (like the cyclostomes) also living on the oysters used as a substrate seem only to be found in brackish water in were able to live and in some cases grow in cold-water regions. conditions more severe than those in which they ordinarily existed. He therefore con- Substrate cluded that it was the larval physiology that Substrate is also extremely important in limited the distribution of these species. determining the distribution of brackish wa- However, at that time, little was known ter ectoprocts, as most species cannot live about the larval biology of the ectoproct without some type of firm support, and groups, and he thought that the two groups many seem to prefer a certain type of sup- most characteristic of brackish water, the port: rock, shell, algae, etc. Rocky, algae- ctenostomes and the membraniporine chei- 52 J. E. Winston lostomes, were alike in having very primi- displays many of these characteristics: tive larvae. The actual situation is more zooids and colonies are small, populations complicated and the patterns of larval distri- are large, the life cycle is short with rapid bution have not yet been fully described. sexual development and high reproductive The membraniporine cheilostomes, are potential to take advantage of favorable characterized by the production of many conditions while they last. Colonies can small eggs which develop into cyphonautes grow and produce eggs in three weeks at larvae able to feed and live in the plankton summer temperatures, and the planktonic for an extended period of time. However, it larvae seem to show some adaptations to appears that among the estuarine members estuarine conditions also, being small and of the group there is a trend toward reduc- perhaps somewhat benthonic in their habits tion of the planktotrophic cyphonautes larva (Dudley 1973a). into short-lived and probably more bottom- While not all brackish water species fit the dwelling forms. The ctenostomes which pro- generalist or opportunist category, as even duce cyphonautes-like larvae, moreover, do in an unstable environment fractions of the not penetrate deeply into brackish water. trophic and habitat resources remain stable Though FlustreUidra hispida, a carnose cten- (Valentine 1972), most of the truly brackish ostome found in brackish water to 10-12%o, water species of ectoprocts seem to have has a larva which is externally rather similar adopted this type of life strategy. to a cyphonautes, this larva lacks an alimen- Among the brackish water ctenostomes, tary tract and can have only a very short colony development appears to be quite planktonic life. The ctenostome genera rapid. For example Menon and Nair (1967) which are most characteristic of brackish noted gonad formation in 20 days in Vlclo- water, Victorella and Bowerbankia, have a rella pavida from the S.W. coast of India. very short-lived larva also. Embryos of this species mature into non- feeding larvae with only a short (few hours) planktonic life before settlement and the Stabiliiy formation of a new colony. It seems that life According to students of ecosytem devel- spans of ctenostomes such as Victorella and opment (e.g., Odum 1969, 1971; Margalef Bowerbankia are, at least under laboratory 1968; Valentine 1971) estuaries can be conditions, shorter than those of estuarine thought of biologically as regions of instabil- cheilostomes such as Conopeum tenuissi- ity both in time and in space. Such regions mum or Meinbranipora tenuis. Unpublished are often characterized by low species diver- laboratory studies made by the author sity, though often the species which are showed that ctenostome colonies developed found occur in high densities. from pieces of stolons on experimental The species able to live under estuarine slides, grew for up to two months, but were conditions have often developed adapta- not able to overgrow the experimental chei- tions which enable them to survive changes lostome colonies {Membranipora tenuis). in their environment: small zooid size, large Eventually the ctenostome colonies died populations (to counteract large mortality and decayed while the cheilostomes flour- due to environmental fluctuation), short life ished. cycles, rapid sexual development and high Schopf (1973) has developed a model of reproductive potential are among those the relationship between the development mentioned (e.g., Pianka 1970). Many of of polymorphism in ectoproct colonies and these same characteristics had been consid- environmental stability. His model predicts ered by other authors to be distinctive to that specialization, with the various func- estuarine animals, but they now appear to tions of the colony being divided among be characteristic of unstable regions in gen- different types of zooids will be favored in eral, rather than just estuarine regions per stable environments, but that in unstable se. areas like estuaries polymorphism will be The membraniporine cheilostome Cono- unrewarding to the colony. From his own peiim tenuissimum, common to estuaries of experience and analysis of the literature he the southeast coast of the United States, concludes that avicularian polymorphism Distribution of Estuarlne Ectoprocts 53

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