Heteropod and Thecosome (Mollusca: Gastropoda) Macroplankton in the Florida Straits

BULLETIN OF MARINE SCIENCE, 49(1-2): 562-574, 1991

HETEROPOD AND THECOSOME (MOLLUSCA: GASTROPODA) MACROPLANKTON IN THE FLORIDA STRAITS

Harding B. Michel and John F. Michel

ABSTRACT Previous areal records of hete:ropod and thecosome molluscs obtained with single- and graded-mesh plankton nets and the Isaacs-Kidd Midwater Trawl (IKMT) are compared with a collection of late juveniles and adults from the Florida Current caught by a MOCNESS- 10 trawl. Sequential depth intervals from the surface to a maximum of 750 m were quan- titatively sampled on transects between Palm Beach, Florida, and Settlement Point, Grand Bahama Island, Bahamas, in August 1978 and February 1979. Of the eight heteropod and 15 thecosome species or formae captured, the most numerous were, in order of abundance, the heteropods Atlanta peroni. Pterotrachea hippocampus. P. coronata and A. inc/inata, and the thecosomes Cavolinia uncinata forma uncinata. Diacria trispinosa and Clio pyramidata. Data on species abundance relative to earlier reports and gear types and on vertical distribution during day and night are presented. No notable evidence of deep-water occurrence was found.

Reports of the occurrence and distribution of pelagic gastropods in the Rorida Current and the contributing currents from the Caribbean Sea and the Gulf of Mexico have been based primarily on collections made with relatively fine-meshed plankton nets. These sample populations of smaller species but often do not capture specimens oflarger ones such as the heteropds Pterotrachea coronata and P. hippocampus, and the thecosomes Clio recurva and Cavolinia uncinata. One purpose of this paper is to give quantitative evidence of incomplete sampling of these forms that, at least as adults, may avoid plankton nets, and also are poorly collected by slow-moving trawls, such as the IKMT, which pass small and inter- mediate sizes and tend to crush larger animals. Another is to describe the com- parative abundance of the larger heteropod and thecosome species obtained in the trawl designed to sample mesopelagic fishes. The literature cited excludes most historical works and consists mainly of recent efforts to approximate abundance and vertical distribution of species. Concerning heteropods, Taylor and Berner (1970) reported relative numbers collected in the Gulf of Mexico by three methods: a l-m net (mesh size 752 /otm),a "Bongo" sampler (mesh size 505 /otm)and a 10-foot IKMT ('14" stretch liner). Michel and Foyo (1976) sampled Caribbean zooplankton in multilevel horizontal tows of75 cm modified "Discovery" nets (graded mesh sizes 3.2 mm, 1.6 mm and 110 /otm), and they recorded numbers of heteropods caught in the comparable tows. Thecosomes have been more thoroughly studied in this area than heteropods. Wormelle (1962) examined samples collected in the Rorida Straits off Miami with the same type of Discovery net described in the previous paragraph. Catches obtained from the Caribbean Sea by Michel and Foyo (1976) formed the basis for Haagensen's thesis (1976). In their zoogeographic and taxonomic review, Be and Gilmer (1977) discussed sampling inadequacies associated with net and mesh size, towing speed and duration, and they referred to Wells' (1973) findings of effects of mesh size on estimates of euthecosome density in the Caribbean off Barbados. Van der Spoel produced extensive compendia on thecosomes (1967) and on thecosomes and heteropods (1976). In addition to a thorough systematic review, these works contain information on anatomy and world-wide distribution. Formae established by van der Spoel, of course, do not appear in the papers of Wormelle

562 MICHEL AND MICHEL: HETEROPOD AND THECOSOME MACROPLANKTON 563

(1962) and Taylor and Berner (1970) and in the review ofheteropods by Thiriot- Quievreaux (1973). In Haagensen (1976) and the present work, formae were assigned in all clear cases. Lalli and Gilmer's (1989) beautifully illustrated and detailed work on the biology of holophanktonic gastropods brings together modem knowledge of the kinds of heteropods and thecosomes and their life styles.

METHODS

The present data were obtained from collections made by Richard H. Backus and James E. Craddock, Woods Hole Oceanographic Institution, Woods Hole, MA. The MOCNESS-lO trawl was described by Backus and Craddock (1982), who used it to sample mesopelagic fishes. On two cruises of R/V OCEANUS,transects were made between Palm Beach, Florida, and Settlement Point, Grand Bahama Island, Bahamas (Table 1). After removing fishes from these tows, Backus and Craddock kindly sent the senior author the remainder of the catch. The circular openings of the MOCNESS-I 0 net are about 3 mm in diameter. The area of the mouth when fishing is approximately 10 m2• Speed during fishing varied from ca. 1.3-2.9 kt. Bottom depths extended from 770 to 360 m, east to west, and fishing depths covered multiple ranges from the surface to 750 m (Table 1). Because the objective was to collect mesopelagic fishes, greater depths and ranges were sampled in the daytime than at night, particularly during the hours around midnight. This sampling bias and the lack of replication permit evaluation of vertical distribution only in general terms. In 1979, heteropods and thecosomes were sorted from the original buffered formalin preservative, used after collection in 1978 and 1979, and stored in 70% alcohol. The condition of the material remains excellent. So few pseudothecosomes and gymnosomes were found in the samples that identification of most species was not attempted. Total counts of the other species and formae were made.

RESULTS AND DISCUSSION A list of the species collected by MOCNESS-IO follows. In Tables 2 and 3, historical and present records are compared. The abundance of heteropod and euthecosome species obtained from the depths sampled at each station appears in Tables 4, 5 and 6.

List Of Species

Class Gastropoda Subclass Prosobranchia Order Heteropoda Family Atlantidae Oxygyrus keraudreni (Lesueur, 1817) Atlanta inclinata Souleyet, 1852 Atlanta peroni Lesueur, 1817 Family Carinariidae Cardiapoda placenta (Lesson, 1830) Carinaria lamarcki Peron and Lesueur, 1810 Family Pterotracheidae Pterotrachea coronata Niebuhr, 1775 Pterotrachea hippocampus Philippi, 1836 Pterotrachea scutata Gegenbaur, 1855 Subclass Opisthobranchia Order Thecosomata Suborder Euthecosomata Family Cavoliniidae Styliola subula (Quoy and Gaimard, 1827) Clio pyramidata Linnaeus, 1767 forma lanceolata (Lesueur, 1813) Clio recurva (Children, 1823) Cuvierina columnella (Rang, 1827) forma atlantica van der Spoel, 1970 Diacria trispinosa (de Blainville, 1821) 564 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Table I. Station data, OCEANUS cmises 49 and 55 between Palm Beach, Florida, and Settlement Point, Grand Bahama Island

OcEANUS 49

Bottom Station Lat. Long. Time Sample depth depth Water filtered number Date N W R (m) (m) (m') 99-0 6 Aug 78 26°42' 79"08' 2103-2258 0-200 580 50,000 99-1 6-7 Aug 78 26°42' 79"08' 2258-0057 200-570-200 580 58,000 99-2 7 Aug 78 26°31' 79°12' 0057-0333 0-200 580 83,000 100-0 7 Aug 78 26°44' 79°23' 0502-0640 0-270 630 41,000 100-1 7 Aug 78 26°44' 79°23' 0640-1010 270-600-280 630 100,000 100-2 7 Aug 78 26°47' 79°25' 1010-1107 290-0 630 33,000 101-0 7 Aug 78 26°42' 79°31' 1231-1320 0-400 770 16,000 101-1 7 Aug 78 26°42' 79°31' 1320-1657 400-750-400 770 107,000 101-2 7 Aug 78 26°38' 79°31' 1657-1755 400-0 770 39,000 102-0 7 Aug 78 26°44' 79°40' 1929-2040 0-520 565 22,000 102-1 7 Aug 78 26°44' 79°48' 2040-2202 550-100 565 47,000 102-2 7-8 Aug 78 26°52' 79°40' 2202-0004 100-0 565 61,000 103-0 8 Aug 78 26°45' 79°44' 0106-0246 0-70 450 58,000 103-1 8 Aug 78 26°45' 79°44' 0246-0425 70-150-80 450 56,000 103-2 8 Aug 78 26°53' 79°46' 0425-0600 80-0 450 60,000 104-0 8 Aug 78 26°42' 79°31' 0836-0940 0-350 770 28,000 104-1 8 Aug 78 26°42' 79°31' 0940-1350 350-710-350 770 134,000 104-2 8 Aug 78 26°37' 79°32' 1350-1444 350-0 770 24,000 105-0 8 Aug 78 26°42' 79°31 ' 1525-1613 0-350 770 22,000 105-1 8 Aug 78 26°42' 79°31 ' 1613-1857 350-700-350 770 85,000 105-2 8 Aug 78 26°39' 79°32' 1857-1941 350-0 770 30,000 106-0 8 Aug 78 26°43' 79°31' 2045-2147 0-200 770 30,000 106-1 8 Aug 78 26°43' 79°31' 2147-2358 210-90 770 74,000 106-2 8-9 Aug 78 26°43' 79°31 ' 2358-0212 90-0 770 76,000

OcEANUs 55 143-0 17 Feb 79 26°41' 79°36' 1405-1521 0-400 720 32,000 143-1 17 Feb 79 26°41" 79°36' 1521-1635 400-650 720 30,000 143-2 17 Feb 79 26°41 ' 79°36' 1635-1720 650-400 720 27,000 143-3 [no specimens] 1720-1754 400-300 720 21,000 143-4 17 Feb 79 26°41' 79°36' 1754-1918 300-150 720 50,000 143-5 17 Feb 79 26°38' 79°36' 1918-2029 150-0 720 46,000 144-0 17 Feb 79 26°44' 79°36' 2122-2301 0-650 680 36,000 144-1 [no specimens] 2301-2356 650-400 680 31,000 144-2 17-18 Feb 79 26°44' 79°36' 2356-0054 400-160 680 33,000 144-3 18 Feb 79 26°44' 79°36' 0054-0148 160-100 680 31,000 144-4 18 Feb 79 26°44' 79°36' 0148-0301 100-50 680 42,000 144-5 18 Feb 79 26°40' 79°39' 0301-0413 50-0 680 35,000 145-0 18 Feb 79 26°43' 79°47' 1327-1430 0-350 360 25,000 [extrapolated] 145-1 18 Feb 79 26°43' 79°47' 1430-1506 340-320 360 19,000 145-2 18 Feb 79 26°43' 79°47' 1506-1557 320-360-310 360 24,000 145-5 18 Feb 79 26°37' 79°51' 1557-1734 310-0 360 50,000 146-0 18 Feb 79 26°42' 79°35' 1906-2207 0-680 750 70,000 146-1 [no specimens] 2207-2324 680-250 750 43,000 146-2 18 Feb 79 26°42' 79°35' 2324-2341 250-200 750 10,000 146-3 18-19 Feb 79 26°42' 79°35' 2341-0020 200-150 750 23,000 146-4 19 Feb 79 26°42' 79°35' 0020-0111 150-100 750 29,000 146-5 19 Feb 79 26°36' 79°30' 0111-0222 100-0 750 42,000 147-0 19 Feb 79 26°35' 79°29' 0312-0419 0-100 710 33,000 147-1 19 Feb 79 26°35' 79°29' 0419-0534 100-200 710 37,000 147-2 19 Feb 79 26"35' 79°29' 0534-0711 200-650 710 39,000 147-4 19 Feb 79 26"35' 79°29' 0711-0802 650-610-650 710 22,000 147-5 19 Feb 79 26"29' 79°27' 0802-1043 650-0 710 105,000 148-0 19 Feb 79 26"42' 79°21' 1230-1334 0-300 630 30,000 MICHEL AND MICHEL: HETEROPOD AND THECOSOME MACROPLANKTON 565

Table 1. Continued

OcEANus 55 Bottom Station La!. Long. Time Sample depth depth Water filtered number Date N W R (m) (m) (m') 148-1 19 Feb 79 26°42' 79°21 ' 1334-1444 300-550 630 29,000 148-2 19 Feb 79 26°42' 79°21 ' 1444-1551 550-500 630 35,000 148-3 19 Feb 79 26°42' 79°21 ' 1551-1742 500-330 630 64,000 148-4 19 Feb 79 26°42' 79°21' 1742-1824 330-150 230 24,000 148-5 19 Feb 79 26°31' 79°21' 1824-1850 150-0 630 15,000

Diacria major (Boas, 1886) Cavo/inia gibbosa (d'Orbigny, 1836) Cavo/inia inflexa (Lesueur, 1813) Cavo/inia /ongirostris forma longirostris (de Blainville, 1821) Cavo/inia longirostris forma limbata (d'Orbigny, 1836) Cavolinia longirostris forma strangulata (Deshayes, 1823) Cavolinia tridentata (Niebuhr, 1775) forma bermudensis van der Spoe1, 1974 Cavolinia uncinata forma uncinata (Rang, 1829) Suborder Pseudothecosomata Family Peraclididae Peraclis reticulata (d'Orbigny, 1836) Family Cymbuliidae Corolla ovata (Quoy and Gaimard, 1832) Heteropoda. -Sixteen species have been reported from the area (Table 2). Ac- cording to van der Spoel (1976), Atlanta gaudichaudi Souleyet, 1852, is probably an Indo-Pacific species, and Atlantic records of it are misidentifications of A. peroni Lesueur, 1817. In their paper on planktonic molluscan distribution in the Middle Atlantic Bight, Vecchione and Grant (1983) recognized the two species but now believe that Atlantic populations may consist only of a highly variable A. peroni, which would account for the clustering of the two species in analyses and the lack of ecological separation (G. C. Grant, pers. comm., 14 November 1988). We have assumed that the seven specimens of A. gaudichaudi recorded by Taylor and Berner (1970) were A. peroni, which also was rare in their collections

Table 2. Records of heteropod species in the Gulf of Mexico, Caribbean Sea and Florida Straits

Taylor and Berner Michel and Foyo Species (1970) (1976) Present data Oxygyrus keraudreni + + Protatlanta souleyeti + + Atlanta peroni + + + A. gaudichaudi + A. /esueuri + A. inclinata + + + A. inflata + A. helicinoides + A.jusca + + Cardiapoda placenta + + + Carinaria lamarcki + + Pterotrachea coronata + + + P. hippocampus + + P. scutata + + P. minuta + Firoloida desmaresti + + 566 BULLETIN OF MARINE SCIENCE. VOL. 49. NO. 1-2, 1991

Table 3. Records of thecosome species and formae in the Caribbean Sea and Florida Straits (Haa- gensen (1976) included records from the Gulf of Mexico)

Wonnelle Haagensen Present Species (1962) (1976) data Limacina retroversa + + L. injlata + + L. lesueuri + + L. trochiformis + + L. bu/imoides + + Creseis acicula + + C. a. f. acicula + C. a. f. clava + C. virgula + + C. v. f. virgula + C. v. f. conica + Sty/iola subula + + + Hyalocy/is striata + + Clio pyramidata + + C. p. f. lanceolata + + C. cuspidata + + C. po/ita + + C. recurva + + Cuvierina columnella + + C. c. f. atlantica + + Diacria trispinosa + + + D. t. f. trispinosa + D. major + + D. quadridentata + + D. q. f. danae + Cavo/inia longirostris + + C. I. f. longirostris + + C. I. f. /imbata + + C. I. f. strangulata + + C. tridentata + C. t. f. bermudensis + C. uncinata + + C. u. f. uncinata + + C. gibbosa + + + C. injlexa + + + C. i. f. injlexa + Peraclis reticulata + + + P. bispinosa + P. moluccensis + P. triacantha + P. apicifulva + Cymbu/ia peroni + Gleba cordata + Corolla spectabilis + C. calceola + C. ovata + Desmopterus papilio + + D. gardineri + + D. intermedia + Th/iptodon diaphanus +

(24 specimens). In contrast, it was the most common atlantid in the MOCNESS- 10 samples. Adult A. peroni, the largest species of the Atlantidae, may be able to avoid smaller nets (Seapy, 1990). Comparing records of species in the area (Table 2), Taylor and Berner (1970), MICHEL AND MICHEL: HETEROPOD AND THECOSOME MACROPLANKTON 567

who used three kinds of gear, reported the greatest number, 13. The Discovery net and the MOCNESS-I0 each caught eight species but only half of them are the same. Summarizing Taylor and Berner's results, the numerically dominant forms in I-m net tows were Atlanta lesueuri (17%), Pterotrachea min uta (14%), P. coronata (7%) and Firoloida desmaresti (28%), totaling 66%; and those collected by the IKMT combined with Bongo tows were Protatlanta souleyeti (10%), A. inclinata (8%), Pterotrachea min uta (11%), P. coronata (10%), P. hippocampus (6%), and F. desmaresti (18%), totaling 63%. In his studies ofpterotracheids off Oahu, Hawaii, Seapy (1985) was unable to separate Pterotrachea hippocampus and P. min uta and he suggested that the latter is a junior synonym of the former. However, the status of P. minuta in the western Atlantic Ocean and the Gulf of Mexico has yet to be assessed. Michel and Foyo's (1976) sampling, while geographically extensive, was limited to horizontal tows. Only tows in the upper 125 m collected heteropods, mainly the common tropical forms, A. peroni (16%), A. inclinata (23%) and F. desmaresti (53%). The most numerous species found in the MOCNESS-I0 tows were A. peroni (33%), A. inclinata (13%), P. coronata (14%) and P. hippocampus (19%). The absence of Firoloida desmaresti, common in the other collections and known to be abundant in the upper 100 m of the Florida Current off Miami (Owre, 1964; personal observations), is puzzling. This is the smallest and most fragile of the pterotracheids. Net avoidance is not a reasonable explanation, and the mesh should have retained a species which can reach a length of 40 mm. Pafort-van Iersel (1983) reported low numbers of F. desmaresti in the mid-North Atlantic and commented on the varying reports of its abundance, from occurrance in swarms to extreme rarity, and speculated on a coast-bound distribution. Two species, Protatlanta souleyeti and Atlanta lesueuri, reported as numerous in the Gulf of Mexico by Taylor and Berner (1970) were not caught by the MOCNESS-IO, probably because of size. According to van der Spoel (1976), the maximum shell diameter of Protatlanta souleyeti is 1.5 mm and that of A. lesueuri is 3.0 mm. Thiriot-Quievreaux (1973) noted that there are few data on vertical distribution, and van der Spoel assumed that the predaceous, highly motile heteropods live in the photic zone because of dependence on optic stimuli. In a single series with opening-closing Bongo nets, Taylor and Berner (1970) found most specimens at 50 and 100 m, fewer at 200 m and only two at 400 m, one each of Pterotrachea coronata and P. scutata. All heteropods collected by Michel and Foyo (1976) were caught either in a surface net or in one towed horizontally at the thermocline, the greatest depth being 125 m. None was found in the many hundreds of casts made at much greater depths. The depth ranges sampled by the MOCNESS-I0 were broader on OCEANUS49 than 55. Most heteropods occurred in tows which passed through the upper 200 m, compared with deeper tows, e.g., 200-570-200 m (Table 4, Sta. 99). Depths were further bracketed on OCEANUS55, and again heteropods generally were most populous in the upper 200 m. However, Pafort-van lersel (1983) contended that the vertical distribution ofCarinariidae and Pterotracheidae is broader than earlier thought, certainly not restricted to the photic zone, and that almost 50% of the populations of some pterotracheid species may occur below 200 m. Her conclu- sions were based on data from 48 samples collected in the mid-North Atlantic Ocean. Present data do not support Pafort-van lersel's findings of substantial populations below 200 m (Table 4). Seapy (R. R. Seapy, pers. comm., 12 February 1989; Seapy, 1990) examined 568 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Table 4. Heteropoda. Numbers' 10,000m-3 of water filtered. Abbreviations of species names: ker, Oxygyrus keraudreni; incl, Atlanta inclinata; per, A. peroni; plac, Cardiapoda placenta; lam, Carinaria lamarcki; cor, Pterotrachea coronata; hip, P. hippocampus; SCU, P. scutata. DIN = DaylNight; + = < 1'10,000m-3

OcEANUSss Depth Time Station (m) (R) DIN ker inel per plac lam cor hip seu 99 0-200 2103-2258 N 1 + + 200-570-200 2258-0057 N + 200-0 0057-0333 N I + 100 0-270 0502-0640 N/D 270-600-280 0640-1010 D 290-0 1010-1107 D 3 101 0-400 1231-1320 D I 400-750-400 1320-1657 D 400-0 1657-1755 D + 2 102 0-520 1929-2040 N + 550-100 2040-2202 N + + 100-0 2202-0004 N + 7 103 0-70 0106-0246 N + 70-150-80 0246-0425 N 80-0 0425-0600 N 5 + + 104 0-350 0836-0940 D 4 350-710-350 0940-1350 D 350-0 1350-1444 D 5 + + 105 0-350 1525-1613 D 2 350-700-350 1613-1857 DIN 350-0 1857-1941 N + + 106 0-200 2045-2147 N 4 + 210-90 2147-2358 N + + + + 90-0 2358-0212 N 2 + + OcEANus 5S 143 0-400 1405-1521 D 2 + 3 + 400-650 1521-1635 D + 650-400 1635-1720 D 400-300 1720-1754 D 300-150 1754-1918 DIN + 2 2 150-0 1918-2029 N I + 4 + 144 0-650 2122-2301 N 2 I + 2 650-400 2301-2356 N 400-160 2356-0054 N I 2 160-100 0054-0148 N I 4 2 100-50 0148-0301 N I I + 3 I 50-0 0301-0413 N 7 5 3 1 + 16 145 0-350 1327-1430 D 4 + + 3 340-320 1430-1506 D I 320-360-310 1506-1557 D + 310-0 1557-1734 D 1 + 2 146 0-680 1906-2207 N + + + 680-250 2207-2324 N 250-200 2324-2341 N 200-150 2341-0020 N + + I 150-100 0020-0111 N + I 6 I 3 100-0 OIl 1-0222 N 8 1 I 4 147 0-100 0312-0419 N 1 I 6 100-200 0419-0534 N I 2 + 2 200-650 0534-0711 N/D MICHELAND MICHEL:HETEROPODAND THECOSOMEMACROPLANKTON 569

Table 4. Continued

OcEANus ss Depth Time Station (m) (R) DIN ker inel per plac lam cor hip seu 650-610--650 0711--D802 D 65O--D 0802-1043 D 1 + + + 148 0-300 1230-1334 D 2 + 300-550 1334-1444 D + 550-500 1444-1551 D 500-330 1551-1742 D 330-150 1742-1824 DIN + 15O--D 1824-1850 N 6 atlantid distribution in a series of replicate Bongo tows from the upper 300 m off Oahu, Hawaii. Atlanta peroni is the only species of the genus common both there and in the MOCNESS-IO samples. During day, Seapy found A. peroni between 300 m and the surface, with maximum numbers in the approximate range 140- 90 m, while at night the populations were concentrated in the upper 140 m. The distribution of this species in the Florida Current seems similar although it cannot be directly compared because of the difference in mesh size (505 .urn vs. 3 mm) and the sampling bias noted in ··Methods." Generally, at night, A. peroni was most abundant in the upper 50, 100 or 150 m; during day, comparable numbers were found in tows through the upper 350 m (Table 4). The MOCNESS-IO caught < 1-8 '10,000 m-3 while the Bongo net used by Seapy collected in about the same numerical range, however, in 1,000 m3 of water filtered. In the two tropica1/ subtropical oceanic areas sampled, this perhaps coincidental 10-fold difference may indicate that the Bongo-collected specimens, rarely exceeding 3.0 mm in shell diameter (Seapy, 1990), may be about 10 times more numerous than the forms in the size range 4.0-8.5 mm caught in the MOCNESS-IO. The eight heteropod species collected are among those known to attain the greatest size in this group of planktonic gastropods. No specimens of the large soft-bodied genera Carinaria, Cardiapoda and Pterotrachea exceeded or even approached the maximum recorded size. For example, the largest individual of the largest species, Pterotrachea coronata, measured approximately 155 mm in length; the recorded maximum size is 260 mm. In the Atlantidae, shell diameter, excluding the extensive but fragile keel, provides the basis for comparative mea- surements. Atlanta inclinata was exceptional in exceeding the maximum recorded size of 5.0 mm (N = 36, range, 4.0-7.5 mm, average diameter 5.3 mm). Mea-

Table 5. Thecosomes rare in MOCNESS-1O collections (N = actual number)

Species Cruise Station Fishingdepth (m) N

Peradis reticulata OCEANUS 49 101-1 400-750-400 1 Corolla ovata 55 144-3 160-100 1 Styliola subula 55 144-4 100-50 1 55 147-0 0-100 6 Cavolinia inj/exa 55 146-0 0-680 1 C. longirostris f. longirostris 49 103-0 0-70 1 C. l. f. limbata 55 144-5 5O--D 9 145-0 0-350 1 146-0 0-680 1 570 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Table 6. Euthecosomata. Numbers' 10,000m~3 of water filtered. Abbreviations of species names: pyr, Clio pyramidata; ree, C. recurva; col, Cuvierina columnella; tri, Diacria trispinosa; maj, D. major, gib, Cavo/inia gibbosa; Ion, C. longirostris forma strangulata; ber, C. tridentata forma bermudensis; une, C. uncinata. DIN = DaylNight. + = < 1·10,000m-3

OcPANUS 49 Station Depth Time number (m) (R) DIN pyr ree col lri maj gib Ion ber unc 99 0-200 2103-2258 N + + + 3 + 23 200-570-200 2258-0057 N + 200-0 0057-0333 N 15 I 27 2 20 100 0-270 0502-0640 N/D + + 5 2 + + II 270-600-280 0640-1010 D + + I + 290-0 1010-1107 D I 7 9 101 0-400 1231-1320 D 2 10 8 400-750-400 1320-1657 D + 400-0 1657-1755 D + + 4 4 102 0-520 1929-2040 N I 5 3 15 550-100 2040-2202 N + + 100-0 2202-0004 N 6 3 50 6 47 103 0-70 0106-0246 N 1 + 2 70-150-80 0246-0425 N 4 + 2 56 + 5 + 127 80-0 0425-0600 N + 1 11 + 164 104 0-350 0836-0940 D 6 2 13 350-710-350 0940-1350 D + + 350-0 1350-1444 D 7 I 2 16 105 0-350 1525-1613 D 6 2 + + 7 350-700-350 1613-1857 DIN + + + 350-0 1857-1941 N 2 17 + + + + 5 106 0-200 2045-2147 N + 39 9 I 37 210-90 2147-2358 N + + 4 7 + 14 90-0 2358-0212 N 5 77 + 3 + 39

OcEANUS 55 143 0-400 1405-1521 D 2 + 2 15 6 400-650 1521-1635 D 9 2 650-400 1635-1720 D 12 + 400-300 1720-1754 D 300-150 1754-1918 DIN 14 + + + 150-0 1918-2029 N I + 34 + + + 4 144 0-650 2122-2301 N 2 + + 13 + + + 6 650-400 2301-2356 N 400-160 2356-0054 N + 3 160-100 0054-0148 N I + I + 100-50 0148-0301 N 30 + + 28 I 2 2 + 16 50-0 0301-0413 N 10 2 3 + 4 19 145 0-350 1327-1430 D 4 + 6 2 + 3 13 340-320 1430-1506 D 2 320-360-310 1506-1557 D 3 + 310-0 1557-1734 D 2 5 2 + 7 146 0-680 1906-2207 N 4 7 I I + 8 680-250 2207-2324 N 250-200 2324-2341 N 200-150 2341-0020 N 3 + I 150-100 0020-0111 N + 6 I I I 3 2 100-0 0111-0222 N 16 1 I 82 I 1 22 147 0-100 0312-0419 N 60 5 3 72 8 33 100-200 0419-0534 N I 2 1 3 5 200-650 0534-0711 N/D + + + I MICHEL AND MICHEL: HETEROPOD AND THECOSOME MACROPLANKTON 571

Table 6. Continued

OCEANUS55 Station Depth Time number (m) (R) DIN pyr rec col tri maj gib Ion ber unc

650-610-650 0711-0802 D 650-0 0802-1043 D 6 + 1 148 0-300 1230-1334 D + + 2 6 300-550 1334-1444 D + 36 550-500 1444-1551 D 1 500-330 1551-1742 D 1 1 + 330-150 1742-1824 DIN 3 + 150-0 1824-1850 N 6 7

surements of 40 A. peroni ranged from 4.3 to 8.5 mm, with an average diameter of 6.3 mm. According to van der Spoel (1976), the maximum shell diameter is 11.0 mm. Order Thecosomata. - Thirteen of the species and formae collected are members of the Suborder Euthecosomata; only two, Peraclis reticulata and Corolla ovata, represent the Suborder Pseudothecosomata (Table 3). Notably absent are species of the euthecosomes Limacina and Creseis reported by Wormelle and Haagensen (Table 3), whose specimens were collected in Discovery nets with graded-mesh sizes from 3.2 mm to 110 ~m. The mesh of the MOCNESS-10, being approxi- mately 3 mm in diameter, does not retain these abundant small forms. The five species of the helicoid-shelled Limacina reported from the area vary in maximum diameter from < 1 to 3 mm. The fragile conical shell of Creseis may grow very long (to ca. 33 mm) but the maximum diameter is only 1-2 mm. Considering the numbers of all species' 10,000 m-3 of water filtered in the 54 samples analyzed, thecosomes fall into three categories of abundance: rare, fre- quent and common. The adult shells of the rare forms, with the possible exception of Styliola subula, are large enough to be retained by the MOCNESS-l 0, and one can only speculate about the causes, aside from patchiness, of such low abundance. The rarities were caught once (Cavolinia injlexa, C. longirostris f. longirostris, Peraclis reticulata and Corolla ovata), twice (Styliola subula) or three times (c. longirostris f. limbata) (Table 5). The last two were the most numerous, each in one sample collected in early morning dark hours from the upper 100 m, with 2.0 and 2.3 specimens' 10,000 m-3 of water filtered. The average abundance of the six rare forms ranged from 0.1 to 1.1'10,000 m-3• The six frequently caught species/formae occurred in 24-52% of the samples and average 1-2 specimens' 10,000 m-3• In order of increasing abundance, they are Cavolinia tridentata f. bermudensis, Cuvierina columnella f. atlantica, Cavo- linia longirostris f. strangulata, Diacria major, Clio recurva and Cavolinia gibbosa. The greatest number obtained on one occasion was nine C. gibbosa'10,000 m-3, from the upper 200 m at night. The common species, Clio pyramidata (present in 63% of samples), Diacria trispinosa (81%), and Cavolinia uncinata f. uncinata (83%), averaged, respectively, 6, 14 and 16 specimens' 10,000 m-3• None of these was numerous in Wormelle's (1962) material, and she commented on the few specimens, e.g., describing C. uncinata as "an uncommon species." The fact that, in their review, Be and Gilmer (1977) reported these and the other species frequently caught in the MOCNESS- 572 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Figure 1. Living Clio recurva, 2.3 em in shell length, with epifaunal hydroids, Campaniclava clionis, X. Photograph by Chris Syms. MICHEL AND MICHEL: HETEROPOD AND THECOSOME MACROPLANKTON 573

10 to be uncommon illustrates the special problems of sampling post-juvenile populations of these forms. In regard to vertical distribution, during OCEANUS49, most euthecosomes were caught in the shallower casts of a series except for Stations 103 and 106 in which all of the tows occurred within the upper 210 m (Table 6). On OCEANUS55, there was a greater number of casts per series and the majority of specimens was found in the upper 150 m at night. Considering only the three common species, data from OCEANUS55 generally support Wormelle's (1962) conclusion that they are diurnal migrators. Clio pyra- midata, Diacria trispinosa and Cavolinia uncinata all were most numerous in the upper 100 m at night. Day catches contained larger numbers of C. pyramidata below 150 m (Sta. 143) and of D. trispinosa below 300 m (Sta. 148). Although C. uncinata was fairly common in day tows that passed through the upper 300- 400 m (Stas. 143, 145, 148, Table 6), there is no clear evidence of population movement to greater depths in these data. Lalli and Gilmer (1989) summarized information on the remarkable hydrozoan epifauna of certain euthecosomes. Although Cuvierina columnella, Diacria tri- spinosa and Cavolinia tridentata are known to be hosts, no hydro ids were observed on the present material. However, all specimens of Clio recurva bore Campani- clava clionis Vanhoffen, 1910. The idenity of the hydroid was determined by W. Vervoort from MOCNESS-10 material which he deposited in the Rijksmuseum van Natuurlijke Historie, Leiden, Netherlands (pers. comm., 1985; Vervoort, 1946). Specimens have also been registered in the British Museum (Natural His- tory) under the number 1985.3.1.1. (Simon J. Moore, pers. comm., 25 March 1985). An individual collected by Michel (1985) from the upper 100 m in the Florida Current off Miami was photographed alive, with hydro ids extended (Fig. 1).

CONCLUSIONS Of the gastropods collected with MOCNESS-IO, 8% are heteropods and 92% thecosomes, all late juveniles or adults and present in low densities ranging from < 1 to 16'10,000 m-3 (heteropods) and to 164'10,000 m-3 (thecosomes). Almost no comparable quantitative data on catches either with the same or different gear exist. The heteropod species represented about half of those previously reported from the area. Only atlantids which may attain 5-11 mm maximum recorded shell diameter were collected. Atlanta peroni and A. inclinata accounted for 46% of total heteropods sampled. Among carinariids and pterotracheids, all too large to pass through the net, only Pterotrachea coronata and P. hippocampus were rela- tively numerous, amounting to 33% of total heteropods. The data thus indicate that the larger heteropod fauna in the Florida Straits consists primarily of these four species with the addition of Firoloida desmaresti, known to be abundant but unaccountably absent from the catches. The 15 thecosome species were categorized as rare (6), frequently caught (6) and common, the latter comprising Clio pyramidata, Diacria trispinosa and Ca- volinia uncinata forma uncinata. The fact that these species are recorded as un- common in previous works, while many genera and species known to be abundant in the area were not caught by the MOCNESS-1 0, demonstrates the impossibility of assessing populations of these molluscs without using a range of mesh sizes and sampling techniques. Because the times and depths of towing were selected for a purpose other than 574 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991 sampling these pelagic molluscs, data on vertical distributiun basically show only that the greatest number were captured in the upper 100 m at night. The best examples were found in tows from OCEANUS 55, Stations 144, 146 and 147, where the counts of total molluscs caught in the four 0-50 and 0-100 m night tows were 161, 141 and 193 '10,000 m-3, respectively. In contrast, fewer animals were found in more numerous (11 vs. 4) tows taken in the afternoon over greater depth ranges. At Station 143, three tows in the range 0-650 m (1,405-1,720) netted a total of 55'10,000 m-3• At Station 145, there were four tows in the range of 0-360 m (1,327-1,734) and total specimens were 65'10,000 m-3• At Station 148, a total of 51'10,000 m-3 were caught in four tows in the upper 550 m between the hours of 1230 and 1742. These figures represent mainly the abundance of thecosomes. However, the data contain no evidence of significant concentrations of either group below approximately 200 m except for indications of diurnal vertical mi- gration by Clio pyramidata and Diacria trispinosa.

LITERATURE CITED

Backus, R. H. and J. E. Craddock. 1982. Mesopelagic fishes in Gulf Stream cold-core rings. J. Mar. Res. 40 (Suppl.): 1-20. Be, A. W. H. and R. W. Gilmer. 1977 A zoogeographic and taxonomic review of euthecosomatous Pteropoda. Pages 733-808 in A. T. S. Ramsay, ed. Oceanic micropaleontology. Academic Press, London. Haagensen, D. A. 1976. Caribbean zooplankton. Part II. Thecosomata. Off. Nav. Res., Dept. of the Navy. U.S. Govt. Print. Off., Washington, D.C. Pp. 551-712. Lalli, C. M. and R. W. Gilmer. 1989. Pelagic snails. The biology of holoplanktonic gastropod mollusks. Stanford Univ. Press, Stanford, California. 259 pp. Michel, H. B. 1985. The fuzzy sea butterfly. Sea Frontiers 31: 181-182. -- and M. Foyo. 1976. Caribbean zooplankton. Part I. Siphonophora, Heteropoda, Copepoda, Euphausiacea, Chaetognatha and Salpidae. Off. Nav. Res., Dept. of the Navy. U.S. Govt. Print. Off., Washington, D.C. pp. 1·-549. Owre, H. B. 1964. Observations on development of the heteropod molluscs Pterotrachea hippocampus and Firoloida desmaresti. Bull. Mar. Sci. 14: 529-538. Pafort-van Iersel, T. 1983. Distribution and variation of Carinariidae and Pterotracheidae (Heter- opoda, Gastropoda) of the Amsterdam Mid North Atlantic Plankton Expedition 1980. Beaufortia 33: 73-96. Seapy, R. R. 1985. The pelagic genus Pterotrachae (Gastropoda: Heteropoda) from Hawaiian waters: a taxonomic review. Malacologia 26: 125-135. --. 1990. Patterns of vertical distribution in epipelagic heteropod molluscs off Hawaii. Mar. Ecol. Prog. Ser. 60: 235-246. Spoel, S. van der. 1967. Euthecosomata. J. Noorduijn en Zoon N.V., Gorinchem, The Netherlands. 375 pp. --. 1976. Pseudothecosomata, Gymnosomata and Heteropoda. Bohn, Scheltema and Holkema, Utrecht, The Netherlands. 484 pp. Taylor, D. and L. Berner, Jr. 1970. The Heteropoda (Mollusca: Gastropoda). Pages 231-244 in W. E. Pequegnat and F. A. Chace, Jr., eds. Contributions on the biology of the Gulf of Mexico, Texas A&M University Oceanographic Studies. Gulf Publishing Co., Houston, Texas. Thiriot-Quievreux, C. 1973. Heteropoda. Pages 237-261 in H. Barnes, ed. Oceanogr. Mar. BioI. Ann. Rev. 11. George Allen and Unwin Ltd., London. Vecchione, M. and G. C. Grant. 1983. A multivariate analysis of planktonic molluscan distribution in the Middle Atlantic Bight. Cont. Shelf Res. I: 405-424. Vervoort, W. 1946. Exotic hydroids in the collections of the Rijksmuseum van Natuurlijke Historie and the Zoological Museum at Amsterdam. Zool. Meded. Leiden 26: 293-294. Wells, F. E., Jr. 1973. Effects of mesh size on estimation of population densities of tropical euthe- cosomatous pteropods. Mar. BioI. 20: 347-350. Wormelle, R. L. 1962. A survey of the standing crop of plankton of the Florida Current. VI. A study of the distribution of the pteropods of the Florida Current. Bull. Mar. Sci. Gulf Caribb. 12: 95- 136.

DATE ACCEPTED: August 27,1990.

ADDRESS: Rosenstiel School oj Marine and Atmospheric Science, University oj Miami, 4600 Rick- enbacker Causeway, Miami. Florida 33149-1098.