BULLETIN OF MARINE SCIENCE, 49(1-2): 638-659, 1991

SPECIES COMPOSITION AND FOOD HABITS OF THE MICRONEKTONIC CEPHALOPOD ASSEMBLAGE IN THE EASTERN GULF OF MEXICO

Kenneth C. Passarella and Thomas L. Hopkins

ABSTRACT Cephalopods are a common but not abundant element of the micronekton of the eastern Gulf of Mexico, an area hydrographically and biologically similar to low latitude oligotrophic oceans throughout the world. Forty seven species were identified from Tucker trawl collections in the vicinity of 27°N, 86°W, with seven new records for the Gulf. All species have been recorded from the Atlantic and 69% are pan-oceanic at low latitudes. The Teuthoidea were the largest fraction of the catch, particularly species of the families Enoploteuthidae and Cranchiidae. All but three species occurred in the epipelagic zone at night and diel vertical migration is suggested for many of the population. Closing trawl data indicate that most of the cephalopod population occurs shallower than 200 m at night and centers at 100 to 400 m during the day. Populations of several of the abundant, smaller species were greatest in July but this could not be linked, on the basis of size measurements, to recruitment of juveniles to the population. Diet analysis indicates that micronektonic cephalopods are crustacean feeders as juveniles, but rely more on fish as they mature (>4 cm mantle length). Some cannibalism is apparent. Cranchiids contained relatively little food which might result from a relatively inactive life strategy. The latter is suggested by rather flaccid musculature in comparison to other teuthoids. The copepod genus Pleuromamma is highly selected for by a number of species, perhaps a function of the strong bioluminescent signal produced by members of this genus. Cluster analysis revealed several feeding guilds among the abundant species, though intracluster diets usually exhibited strong overlap. Given the relatively low abundance levels of cephalopods (50-70-lO^km"^; 0-1,000 m), trophic competition may stem primarily from more abundant ( > 1 0 x) micronektonic groups such as midwater fishes and shrimps than from other ceph­ alopods.

Cephalopods are a conspicuous element of the oceanic fauna, ranging in size from planktonic to some of the largest of nekton (Roper et al., 1984). We report herein on the micronektonic component of the pelagic assemblage in the eastern Gulf of Mexico. Composition of the fauna in this region is fairly well known through the efforts of Voss and his colleagues (Voss, 1954, 1956a, 1956b, 1962, 1963a, 1964; Voss and Voss, 1962; Roper, 1964; Roper etal., 1969;Caims, 1976) and from Lipka’s (1975) dissertation research. The present work is based on two large collections made with opening-closing Tucker trawls in the vicinity of 27°N, 86®W in a water depth of 3,200 m. The first sample set is from 1975-1977 R/V Columbus Iselin cruises during which 20 depth horizons were sampled day and night. These collections provided diel vertical distribution information in the epi- mesopelagic zone (0-1,000 m). The second set comes from 1984-1987 R/V SuNCOASTER cruises which concentrated on the upper 200 m at night. Samples from these cruises were used to further examine vertical distribution patterns in the epipelagic zone and especially for cephalopod trophic studies. Since little has been reported on diets of micronektonic cephalopods, the present results have special value in elucidating their role in oligotrophic tropical-subtropical ecosys­ tems.

M e t h o d s

Sampling took place within a 20 km circle centered at 27°N, 86°W. Collecting gear on RA'C o l u m b u s Ise lin cruises was 3.2 and 6.5 m^ nets (Tucker trawl) o f 4 mm mesh, with a 1 mm mesh codend.

638

DWH-AR0127433 PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 639

Trawls were opened and closed with messenger-operated, double-trip mechanisms, and volume of water filtered was measured with dial-type meters which recorded only when the net was fishing (Hopkins et al., 1973). Depth was monitored through a deck readout using a depth transducer con- ducting-cable-system. A depth trace of each tow was obtained with a time-depth recorder, Trawling speed was 1.5 to 3.0 kn. A coarse mesh (4 mm) “fishcatcher” sleeve was inserted in the trawl body ahead of the codend net to retain micronekton while allowing zooplankton to pass through to the codend. This was done to minimize bias in diet analysis resulting from post-capture feeding in the trawl (Hopkins and Baird, 1975). Also, collapsible 44-44 cm or 66-66 cm, 163-^rm mesh plankton nets were suspended in the mouth of each trawl to capture zooplankton concvnrently with micronekton. Flowmeters used with the plankton nets recorded only when the nets were open. Similar Tucker trawl-plankton net com­ binations were used on R/V Su n c o a ste r cruises, thou^ with the addition of a 3.2 m^, 1.6-mm mesh trawl and the substitution of clock release mechanisms (Davies and Barham, 1969) for the messenger operated net releases. R/V Columbus Iselin tows were at discrete horizons and had a depth variance of ± 15 m at depths <300 m and ±25 m at greater depths. R/V Suncoaster tows were of two kinds, 0-200-0 m oblique sweeps and 25 to 50 m discrete zone hauls in the upper 200 m. A summary of the collection data is in Passarella (1990). Samples were initially preserved in 5-10% v/v formalin-sea water solution buffered with borax and subsequently transferred to 50% isopropanol. Cephalopods were sorted to species in the lab and mantle lengths (ML) were measured. Most (>95%) of the individuals in our collections were micronektonic in size, 0.5-20.0 cm ML, though the larger cephalopods were included in the study to provide additional information on species composition, vertical distribution and feeding habits of the assemblage. The protocol for biomass determination was to first weigh alcohol preserved specimens (=AW), soak them in water for 24 h, then reweigh (=WW). Regressions of WW on ML were established for five of the numerically dominant species (Pterygioteuthis gemmata, P. giardi, Pyroteuthis margaritifera, Heli- cocranchia pfefferi and Egea inermis), the P values ranging from 84 to 99%. Individuals of less abundant species were weighed separately, with their weights adjusted to WW using a WW = 1.4 AW correction factor. For diet analysis, the cephalopods examined were subdivided into four size classes based on mantle length, < 1 cm ML, 1-2 cm ML, 3-4 cm ML and >4 cm ML. Within each size class digestive tracts (esophagus, stomach, caecum and intestine) were removed and gut contents were distributed as evenly as possible in water on a microscope slide. Examination was at 100 to 400 k magnification. Food, mostly crustacean, was fragmented, therefore prey identification was usually based on diagnostic body parts, In most instances prey were identified to family; often it was possible to classify prey to species and to determine their numbers. In the case of the copepod genus Pleuromamma. the metasomal organ (spot) was measured and its shape recorded to estimate copepod size (using a spot dimension- copepod length regression) and to determine species. Statistical treatment of the data included using the Kolmogorov-Smimov test (Sokal and Rohlf, 1981) in comparing catches of cephalopods by trawls of different meshes (1.6 mm and 4.0 mm). ANOVA statistics were applied to seasonal data (R/V SLntcoASTER collections) to discern significant population size changes in the upper 200 m at n i^ t from cruise to cruise. This was done for three of the most common species,Pterygioteuthis gemmata. P. giardi and Pyroteuthis margaritifera. ANOVA was also used to test differences in mantle length of these three species from cruise to cruise to determine if there were seasonal recruitment patterns. Diets of seven of the abundant species were compared with the Bray-Curtis similarity index (Bray and Curtis, 1957). This index was applied to percent values for each of 21 diet categories where the number of items in each category was expressed as a percent of the total food items recorded for the sample. The similarity indices were then grouped by average distance linkage cluster analysis (Sarle, 1982; Field et al., 1982; Romesburg, 1990) to discern feeding guilds. The cutoff for diet dissimilarity was arbitrarily set at two thirds of the total average linkage cluster distance. Diet diversity was calculated with a variant of the information measure (Travers, 1971); D = 1/N [loga N - 2 n, log; n,] where N = total incidences (=100%) of all food categories (21), n, = incidence (%) of a single food category and D = 0-4.45. Physical data at 27°N, 86°W were obtained through numerous XBT casts on R/V C o lu m b u s Iselin cruises, and from XBT and CTD casts on R/V Su n c o a st e r cruises.

R e s u l t s Hydrography. — The dominant but variable feature of the eastern Gulf circulation is the Loop Current. It is the anticyclonic extension into the eastern Gulf of Mexico

DWH-AR0127434 640 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991 by Caribbean water which forms the Florida Current. The core of the Loop which centers at -2 0 0 m, is characterized by high salinity, >36.5%o, and warm tem­ peratures, >22® (Nowlin, 1971). The surrounding residual water in the eastern Gulf is both cooler and less saline. Intrusion into the Gulf, which is intermittent and unpredictable, is on an axis oriented from the center of the Yucatan Straits to the mouth of the Mississippi (Maul, 1977; Molinari and Mayer, 1980; Sturges and Evans, 1983). Models indicate that at 27®N, 86®W, the Loop Current can be encountered 20 to 30% of the time (Science Application International Corporation, 1989), though our physical data show we encountered the Loop only once in 9 cruises. The great majority of our sampling, then, was in residual eastern Gulf water which maintains its physical integrity to a large degree when the Loop is present. It is estimated that mixing of residual eastern Gulf and the Loop Current waters is no more than 10% (G.A. Maul, NOAA-AOML, personal communica­ tion). The general biological characteristics of residual water are largely shared with those of the Loop Current in that primary production is low (~50 g C m^ yr“'; El-Sayed, 1972) as is zooplankton biomass (1.2 g DW-m"^ over the upper 1,000 m; Hopkins, 1982). Faunal diversity is high, with little difference in species com­ position between Loop Current and residual Gulf water (Michel and Foyo, 1976; Hopkins, 1982; Gartner et al., 1987). Taxonomic Composition.—A total of 2,215 cephalopod individuals were sorted from our collections (Passarella, 1990). At the ordinal level the Sepioidea ac­ counted for 0.8% of the catch, Teuthoidea 89.8%, Vampyromorpha 0.3% and Octopoda 8.6%. Individuals too damaged for identification totalled 0.5%. Among the four orders were 39 genera in 22 families. Forty seven species were identified, though some designations remain uncertain (6 spp.). These include Onykia car- riboea (?), Megalocranchia maxima (?), Mastigoteuthis sp., Leachia sp., Octopus sp. A., and Octopus sp. B., Octopus sp. A had some characteristics in common with O. teuthoides, a species known only from the southwest Pacific (Robson, 1929; Voss, 1963b). Seven species are new records for the Gulf of Mexico; Het- ewteuthis dispar, Lampadioteuthis megaleia, Ancistrocheirus lesueuri, Tanangia danae, Discoteuthis discus, Chiroteuthis capensis and C. joubini. Abundance and Vertical Quantitative estimates of micronekton populations are gear dependent. Consequently, we compared cephalopod catches from trawls of diflFerent mesh size (4 mm vs. 1.6 mm). These comparisons, while they do not assess losses from avoidance by larger cephalopods, do measure escapement through trawl meshes of the sm^ler size classes (Fig. 1). The Kol­ mogorov-Smimov test applied to the data in Figure 1 indicates that at sizes smaller than 8-12 mm ML, the 1.6 mm mesh caught significantly (P < .002; N = 40, 13) more individuals (Fig. 1). Catches by the two meshes of size classes larger than 12 mm ML were not significantly different (P > 0.01; N = 28, 48). There was a precipitous drop in catch per volume filtered for both mesh sizes of ceph­ alopods with mantle lengths <4 mm. This size fraction includes larval stages that are sufficiently small to escape through even 1.6 mm meshes. In calculating abun­ dances in this study only 4-mm mesh-catches were used, as all of the R/V C o lu m b u s I s e l i n series, which yielded the most complete vertical distribution information, were made with nets of this mesh size. Also, abundance data reported by others (see Discussion) are based on midwater trawls of similar mesh size. The five most abundant species on the basis of volume of water filtered were Pterygioteuthis gemmata (10.4-7.6-10^ ’km"^), Pyroteuthis margaritifera (4.1-12.1 • 10^-km“^),Helicocranchiapfefferi{2.2-\.0.0- W km~^),Pterygioteuthusgiardi(6.i-

DWH-AR0127435 PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 641

0 Q 1.6mm MESH (68 TOWS) o VOL FILTERED 9.0x 10“

4.0mm MESH (61 TOWS) -I 3.0 VOL FILTERED 15.1x10“

2.0

0-4.0 4.1 8.1 12.1 16.1 20.1 >24.0 - 8.0 - 12.0 -16.0 - 20.0 -24.0 MANTLE LENGTH SIZE CLASS (mm) Figure 1. Comparison of cephalopod catches in 0-200-0 m nighttime sweeps made with Tucker trawls of different mesh sizes.

2.2-10^-km“^) and Egea inermis (5.8-1.7-lO^ km"^); the ranges represent day and night values for the upper 1,000 m. Total cephalopod abundance in the 0— 1,000 m zone was calculated at 66.9' lO^ km"^ and 58.1 • 10^'km”^, respectively, for day and night. T he five dominant species comprised 44% of the daytime and 59% of the nighttime catches. Biomass rankings (day-night values) of these species were P. margaritifera (0.3-6.2 kg WW-km"^), P. gemmata (1.4-1.7 kg WW- km”^), P. giardi (0.8-1.3 kg WW-km'^), E. inermis (1.4-0.6 kg WW-km'^) and H. pfefferi (0.2-0.9 kg WW-km“^). Total cephalopod biomass was estimated at 10.1-42.0 kg WW-km“^ for day and night, respectively, with the five numerically dominant species contributing 42% of the daytime cephalopod biomass but only 14% of that for night. The small nighttime percentage results from appearances of less common species with much larger specimens in our nighttime catches. Cephalopod biomass in the epipelagic zone (0-200 m) increased from 1.5 kg WW • km“^ during the day to 28.4 kg WW km“^ at night, which results from the com­ bined effect of migration into the mesopelagic zone at night and probably from more successful avoidance of our trawls in shallow waters during the day. Population size of three of the abundant species, Pyroteuthis margaritifera, Pterygioteuthis gemmata and P. giardi demonstrated significant intercruise vari­ ation (ANOVA; P < 0.05; df = 5; F = 2.74-5.22) in the upper 200 m at night, with maxima being 7 to 20 times the minima. The maximum for each of these three occurred in July (Fig. 2), although May estimates for P. gemmata were high as well. However, ANOVA {P < 0.05; df = 5; F = 0.75-1.35) comparisons of mantle lengths among cruises yielded no significant variations, hence seasonal patterns of recruitment of juveniles to the population could not be discerned.

DWH-AR0127436 642 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

30 P. gemmata E I RANGE E • MEDIAN 15 I J I I 0 . p'l Q E 20 > ^ 10 i s X 0 -S. .S.

E 30 p. margaritifera E 15 \ I \ CM 0 d E 20 > ^ Q o 10 _ s s s . J3_

P. giardi

Q E 20

Q 6 10

JAN MAR MAY JUL SEP NOV SAMPLING MONTH Figure 2. Intercruise variations of cephalopod populations in the upper 200 m at night.

Vertical distributions of individual species could not be treated in great detail because of small sample sizes. Daytime catches in most cases were quite small. Distributions of 43 of the species in terms of presence or absence are in Table 1. The salient feature is that 41 of these species were taken in the epipelagic zone at night. The three remaining species, Vampyroteuthis infernalis, Bathyteuthis abyssicola and Joubiniteuthis portieri, were collected only during the day at depths below 500 m. Eight species, listed from Mastigoteuthis sp. through Japetella diaphana in Table 1, showed relatively broad vertical distributions day and night. In the case of four of these, Octopoteuthis megaptera, Ancistrocheirus lesueuri, Pterygioteuthis gemmata and J. diaphana, daytime occurrences were deeper. Fif­ teen species were found only in the upper 300 m at night but at various depths from 100 to 1,000 m during the day. These include the species listed in the table from Histioteuthis c. corona to Ornithoteuthis antillarum. The remaining 18 spe-

DWH-AR0127437 PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 643

Table 1. Cephalopod vertical distribution in the vicinity of 27°N, 86°W. X = night; O = day; T = twilight. Four species, Spiruta spirula, Abraliopsis pfefferi, Bathothauma and lyromma Galiteuthis armata, are not included in the table because they were taken in non-closing trawls covering large vertical ranges (>500 m)

Depth (m) 600- 700- 800- 900- Species 0-100 100-200 200-300 300-400 400-500 500-600 700 800 900 1,000 Vampyroteuthis infernalis — — — — — o o o — o Bathyteuthis abyssicola o — Joubiniteuthis portieri Mastigoteuthis sp. X X _ _ o xo o _ X Egea inermis X xo 0 0 o o — — X — Octopoteuthis megaptera X X — — — xo o — — — Ancistrocheirus lesueuri X X — — — xo o — — — Abraliopsis atlantica X X — — o xo — — — — Pyroteuthis margaritifera X X xo o xo Pterygioteuthis gemmata X xo XO o xo o o — _ _ Japetella diaphana X xo xo xo — o o o — o Histioteuthis c. corona X X x — o o o — — — Cranchia scabra X xo — — — — — — o o Octopus sp. B X X — — — 0 _ o o — Helicocranchia pfefferi — xo o 0 — 0 0 — o — Histioteuthis dofteini X X — o o o o o — — Abralia redfieldi X X o o o 0 o — — — Scaeurgus unicirrhus — X — o o 0 0 — — — Megalocranchia maxima (?) X X — — o 0 0 — — o Selenoteuthis scintillans X xo — — — 0 o — — — Alloposis mollis X X — — o o o — — — Abralia veranyi X X — — — o _ — _ _ Octopus deflippi X X — — — o _ _ — — Pterygioteuthis giardi X xo o o o Ornithoteuthis antillarum X xo o o — iMmpadioteuthis megaleia X X X Argonauta argo X X Brachioteuthis riisei X X Chiroteuthis capensis X X Chiroteuthis joubini X X — Ctenopteryx sicula X X Discoteuthis discus X X Enoploteuthis anapsis X X Enoploteuthis leptura X X Heteroleuthis altantis X X Heteroleuthis dispar X X Leachia sp. X X Onycholeuthis banksii X X Onykia carriboea X X Tanangia danae X X Thysanoteuthis rhombus X X Ommastrephes pteropus X Liocranchia reinhardti X Octopus sp. A T

cies were collected only in the epipelagic zone at night, except for Octopus sp. A which occurred in a twilight tow from this zone. The vertical distribution pattern based on the entire discrete haul catch (Fig. 3) shows that during both day and night, highest densities were in the upper 200 m, with the nighttime maximum the greater. Daytime densities declined more slowly with depth than at night, with a substantial portion (42%) of the population during the day occurring between 200 to 400 m.

DWH-AR0127438 644 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

INDIVIDUALS/lO^m^ 2 0 2 0 100 I, 200 3 0 0 1 . ^ 4 0 0 X I - 5 0 0 Q_ LU 6 0 0 70 0 8 0 0 90 0 DAY NIGHT 1000 Figure 3. The vertical distribution of the micronektonic cephalopod population in the 0-1,000 m zone based on opening-closing Tucker trawls.

Feeding. — Cephalopods often were alive in our catches, hence there was potential for post-capture feeding in the net (Testaverde, 1977). We examined samples from both the trawl codend and the “fishcatcher” sleeve, which allows most plankton­ sized food to pass through to the codend. Comparison of gut contents shows little evidence of feeding in the net, at least in terms of percent of diet overlap or number of items per gut (Table 2). Consequently, the diet analysis results in Table 3 are considered to be representative of natural diets of the cephalopod community in the eastern Gulf of Mexico. A small sample (10 specimens) of sepioids was available and the one species examined, H. dispar, had a crustacean/fish diet which differs little from that of the teuthoids (Table 3). The teuthoids were the most abundant cephalopods in our catch and species of this order, particularly Selenoteuthis scintillans, Abralia redfieldi, Abraliopsis atlantica, Pyroteuthis margaritifera, Pterygioteuthis gemmata and P. giardi, yield­ ed most of the information about diet. Copepods were the numerically dominant food, with the metridiid genus Pleuromamma the major diet item (Table 3).

Table 2. Comparison of diets and gut fullness of cephalopods retained in the coarse mesh (4 mm) fishcatcher sleeve and in the codend plankton net (0.5 mm mesh). Diet overlap measured with the Bray-Curtis similarity index, with diet items assigned to the food categories in Table 5

X no. fooditems/gut

Codend plank­ Fishcatcher Species Size class % Diet overlap ton net sleeve

Abraliopsis atlantica 1-2 cm ML 76 1.3 1.3 Pyroteuthis margaritifera 1-2 cm ML 95 14.5 15.8 Pterygioteuthis giardi 1-2 cm ML 80 6.0 7.1 Selenoteuthis scintillans 1-2 cm ML 90 4.8 4.8

DWH-AR0127439 Table 3. Cephalopod diet composition. Size class code; 1 = < 1 cm ML; 2 = 1-2 cm ML; 3 = 3-4 cm ML; >4 = >4 cm ML

oS. O 'g(j Sam - ■3 .g e Size pie 5 class size < 6

Heteroleuthis dispar 2 6 - - - 1 - 1 1 1 1 _ 2 - - - - - 1 4 4 - - - _____ ii___ - 2 Selenoteuthis scintillans 1 19 1 2 1 4 - 3 4----11---1 - 1 - 2 2 27 6 11 6 36 - 38 - 2 1 1 2 19 - - - 1 - 1 - 7 > _____ !____ > Lampadioteuthis megaleia 1 1 - - - z 2 5 - - o Enoploteuthis anapsis 2 1 none X o■c 3 4 z: Enoploteuthis leptura 1 1 1 - Crtz 2 3 O 3 3 c > 4 2 Abralia redfieldi 1 50 3 7 - 3 1 - X 2 23 1 6 20 > 3 5 - 2 5 r O'T3 > 4 2 o Abralia veranyi 1 none D 2 _ 1 > 3 none Abraliopsis atlantica 1 none 2 46 2 4 6 21 _ 8 5 - 1-3-9 - - 1 1 - 3 10 - 1 - 1 _ 1 ------3 > 4 1 _ _ 1 _ _ 1 Pyroteuthis margaritifera 1 37 - - 1 8 2 200 2 - 1 - 2 38 4 1 5 25 3 462 2 - - - 1 - 50 - - - 1 3 4 - - - 2 - 83 ------4 - - - 1 > 4 ______1 1 - - Pterygioteuthis gemmata 1 58 - 17 16 12 - 18 36 19 4 1 2 2 57 3 13 16 11 2 300 15 5 10 1 26 3 18 1 3 6 5 - 99 2 1 4-17

I > O K)

O Table 3. Continued

Sam - T3 3 Size pie c class size < <3 O w

Pterygioteuthis giardi 2 39 - 2 2 12 1 203 3 - - - 32 - 1 1 1- 34 ______!______Chiroteuthis capensis > 4 1 none Chiroteuthis joubini >4 4______4 Mastigoteuthis sp. 37______>4 8------!______! Cranchia scabra 1 12 none 2 18 none 3 1 5 - - - 3 - - >4 6- -- -- ______!______1 Leachia sp. 1 4 none 2 8 none > 4 25 none Liocranchia reinhardti 2 2 none Bathothauma lyromma > 4 2_-_- - ______!_____ l_l Egea inermis 15_____ 2 10 none 3 11 none > 4 10______1 _3 Galiteuthis armata > 4 2 none Helicocranchia pfefferi 1 6 none 2 16 none 3 7 none > 4 4 none Megalocranchia maximal?) 2 1 none 3 2 none >4 4______!_____ !______!

I > O K) Table 3. Continued

Sam- 2 Size pie e- >.H. class size d 6 X Vampyroteuthis infernalis 1 1 1 2 1 1 3 1 none > 4 I 1 Alloposis mollis 1 7 1 2 4 1 - 1 2 2 Octopoteuthis megaptera 1 6 1 2 11 none > 4 8 1 Tanangia danae 1 1 none 3 3 none Onycholeuthis banksii 1 24 - 1 — 1 — — — — — — — — 5 — — — — — — — / 2 27 — — — 1 — 1 1 — — — — — 4 1 — — — — — — 8 Onykia caribboea 1 10 — — — — — — 2 — 1 — — 1 2 — — 1 2 — — — — Histioteuthis c. corona 1 6 1 1 1 1 2 12 6 - — — — — 1 — — — 1 — 4 — — — — — — — 4 3 1 1 1 1 > 4 1 1 Histioteuthis dofleini 1 14 2 - — 2 — 8 — — — — — — — — — — — — — — — 2 12 5 - — 1 — 7 I — — — — — 4 — — — — — — — 1 3 6 ______4 _ — — _ _ — 3 — — — — — — — __ > 4 3 1 3 Ctenopteryx sicula 1 2 none 2 3 none 3 3 1 I 1 > 4 1 none Brachioteuthis riisei 1 1 none 2 3 none 3 4 none > 4 3 none

0

1 > o K)

K) Table 3. Continued

s 2 E ■o V) x> V a a cl « u c A _o o *o c 4) D 1 3 j= o "o « n *2 >> •o •u S o. a •o u d 'C U y, u o o a c 0 cd S am ­ •a f •C u o J= u o c u £ & j E g a £ a Size ple s u o 1 : o. V a 1 JS class size < w 6 s s o u o d 6 X U 6 U 0 u 6 £

Ommastrephes pteropus > 4 3 8 Ornithoteuthis antillarum 1 29 2 I 1 2 — 2 6 — 5 1 12 2 2 26 2 - 3 none > 4 Thysanoteuthis rhombus 1 none 2 none Japetella diaphana 1 14 2 11 5 1 - ~ - 1 3 - 3 > 4 1 none Argonauta argo 1 14 1 2 1 1 — 1 Octopus defilippi 1 10 1 Octopus sp. B 1 43 Scaeurgus unicirrhus 1 2 2 2

a

I > o K) PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 649

p. I’emmata 6 % 2 ' A '//Mh 9,73%///

w m m m f ...133 f ...-4 15

P. margaritikm KEY 1/555 METHIDIIDAE /\9 % \ pM “ f lim nim am mu s p p 1 [5 || OTHER COPEPODS ///.A7//7, 'f//gw% [555] EUPHAUSilDS ilii HEH FOOD ITEMS

C-.M O OF G U T S EXAMINED F -5 5 5 F-.MO, FOOD ITEMS

lOmmML i0^20mmML 20-30m m M L

Figure 4. Intraspecific diet changes related to ontogeny.

Euchaetid copepods were important as well. Euphausiids, while less frequent food than copepods, probably are important energetically, given their larger size. Thirty six incidences of fish were recorded in teuthoid stomachs, most of these from squid larger than 3 cm ML. Several instances o f cephalopod cannibalism also were recorded. The eight cranchiid species examined, in contrast to most other teuthoids, contained relatively little food. The four vampyromorph specimens analyzed yielded a total of three food items: an Oncaea copepod, an ostracod and most of a small physonect siphonophore colony. Ninety eight octopods were dissected, the majority of which were Octopus sp. B. Forty four different items of food were identified from 32 stomachs containing food, o f which 49% were euphausiids. Fourteen percent o f the prey were fishes and in contrast to the Teuthoidea, only 7% were copepods. The remaining 31% was other crustaceans (11%), molluscs other than cephalopods (11%) and chae- tognaths (9%). Change in diet with growth of cephalopods is expected and this is apparent from Figure 4. Analyses of Pyroteuthis margaritifera and Pterygioteuthis gemmata, the two species with abundant diet information for several size classes, reveal that larger prey, euphausiids in particular, become more important with growth. Also, a large change in numerical proportion of metridiid copepods in the diet occurs during growth from size class 1 to size class 2 in P. gemmata. Information on diets from Table 3 for the seven species with abundant data was subjected to hierarchical cluster analysis to discern feeding guilds. Since ontogenetic changes in diet occur (Fig. 4), data were partitioned by size class, giving multiple entries for most of the species. Four clusters are readily apparent at the 0.8 level in the dendrogram (Fig. 5). Cluster I is a single size class (1) of Pterygioteuthis gemmata. This class had a varied diet, mostly of copepods other

DWH-ARO127444 650 BULLETIN 01- M ARINE SCIENCE, VOL. 49, NO. L-2, 1991

cn cc LU

0 . 8 - o LU 2 g s 0.6 < LU

0 . 4 LU CO 0.2

SIZE I I CLASS (1)(1)(2)(2)(2)(3)(1)(1)(1)(3)(2)(2)(3)(1)(2)(3)

3.0o o2.6„ r,3.0n ^2.00 q0.8„ o0.7, ^0.7 „ 1.7 DIET 3.3 2.9'^'^2.6 2.8^°0.B 1.3 1.6 DIVERSITY 2 2

3 c ?3 c 3 a 3 2 ^ Q Q • - s A A - 0 0 ^ “^ 00 Cio ^ SPECIES 5 r* ^ C i** isT -S ■Ki § ^ OJ a Q 55 ^3 6 c V, C3 '£^ *5^ S 0.; X X X 1 V / CLUSTER 1 II Figure 5. Feeding groups among 7 abundant cephalopod species based on hierarchical cluster analysis of diet composition (see Methods). Size classes: 1 = < 1 cm ML; 2 = 1-2 cm ML; 3 = 3-4 cm ML. than metridriids. Cluster II encompasses various size classes of three species, Abralia redfieldi, Selenoteuthis scintillans and Abraliopsis atlantica. The prevalent food types were euchaetids and metridiids {Pleuromamma spp.), each consisting of 24% (x). Euphausiids were important as well (x = 15%). Cluster III includes two size classes, one each of S. scintillans and Ornithoteuthis antillarum. The numerically important food items for this pair were non-metridiid copepods (x = 39%) and euphausiids (x = 36%). Species in Cluster IV, the largest group, fed mostly on metridiid copepods, 71 to 100% of their diets. Diversity values indicate moderately diverse diets (D = 2.6-3.3) for species in Clusters I-III and low diversity (D = 0-1.7) for Cluster IV. The relative monotony within Cluster IV comes from the predominance of Pleuromamma spp. in diets. Intracluster variation was examined by comparing the size and species com­ position of Pleuromamma in diets of cluster IV cephalopods (Table 4). This was done to determine if a more subtle diet partitioning occurs than could be detected from analysis of the relatively broad food categories in Table 3. The similarity

DWH-ARO 127445 PASSARELLA AND HOPKINS; GULF CEPHALOPOD ASSEMBLAGE 651

Table 4. (A) Composition ofPleuromamma copepods in diets of cephalopod species in diet cluster IV (see Fig. 5). Pleuromamma <2 mm are mostlyP. gracilisariA P. piseki\ those 2-3.5 mm arc virtually all P. abdominalis-, individuals >3.5 mm are P. xiphias. (B). Bray-Curtis similarity index (%) matrix for A

A. Pleuromamma size (mm) Species class guts <2 2-3.5 >3.5 ...... % ■ Pterygioteuthis giardi 1 30 50 50 0 2 314 49 46 5 3 34 21 76 3 Pterygioteuthis gemmata 2 423 49 49 2 3 140 24 73 4 Pyroteuthis margaritifera 1 198 23 72 6 2 425 10 77 12 3 46 0 76 24

P. giardi P. gemm atta p. margaritifera 1 2 3 2 3 1 2 3 P. giardi 1 P. giardi 2 95 P. giardi 3 71 70 P. gemmata 2 98 96 72 P. gemmata 3 74 74 97 75 P. margaritifera 1 73 74 95 74 98 P. margaritifera 2 61 62 90 62 87 88 P. margaritifera 3 50 51 79 51 77 78 89

matrix in Table 6 indicates moderate to strong (>67%) diet overlap in all but 5 of 28 pairings and all similarity indices within this matrix exceed 50%. Diel feeding patterns for six of the abundant teuthoid species (Fig. 6) suggest that feeding occurs throughout the diel period and no feeding cycle was statistically demonstrable. The results were weakened to some degree by small sample size in some time periods, and no data at all were available for the 0500-0800 twilight period. To accommodate the uneveness in sample size for individual species, data were pooled for all six species in Figure 6. Averaged results indicate gut fullness was least for size class 1 in the period 0000-0500 h and 1200-1700 h, and for size class 2, 0000-0500 h.

D is c u s s io n The Gulf Assemblage.— cephalopod fauna of the eastern Gulf of Mexico is an extension of the Atlantic assemblage in that all 43 taxa identified to species have been recorded from the Atlantic (Nesis, 1987; Roper et al., 1984). Twenty five species (57%) are world wide (Nesis, 1987), a pattern reflected as well in two other speciose and dominant elements of the micronekton, the midwater fishes and shrimps. Of the 49 myctophid species identified from the eastern Gulf, 69% are found in all oceans at low latitudes (Backus et al., 1977; Gartner et al., 1987) and of the 25 penaeid species, 60% are cosmopolitan in low latitudes (Burkenroad, 1936, 1940; Foxton, 1970; Donaldson, 1975; Walters, 1976; Kensley, 1981; Hef- feman and Hopkins, 1981; Flock, 1989). The eastern Gulf faunal assemblage,

DWH-ARO 127446 652 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

P. gemmata 12 (16) ( 12) (9) 8 (9) ( 10) (16) (23) 4 ( 2 ) (19) (3) ND -JEU A. redfieldi (5)

( 8) (14)(®) (9) (16) (3) —ta. _ a ND (3) JL P. margaritifera 20 ( 15 ) (3) h- (6)

( 8) o 10 (16) ,(i') ( 10) ( 2 ) (T a ND -A. LU n Q. 20 P. giardi CO (8) (9) ( 2 ) UJ 10 (3) H ( 24) n ND JL Q o S. scintillans (2) o 15 LL 10 IX (4) ( 8 ) (7)

( 6 ) (6) ( 6) (5) -A ND n

(9) A. atlantica 20 (13) ( 6 ) ( 8) 10

ND (5)

AVERAGE VALUE (N=6 spp)

8 -

4

ND 1700- 2000- 0000- 0500- 0800- 1200- 20000 OOOOtl 05000 08000 12000 17000

Figure 6. Diel feeding patterns of 6 cephalopod species. Hatched bars = size class 1 and open bars = size class 2 (see Table 5). Number above bar is gut sample size. N D = no data.

DWH-ARO 127447 PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 653 then, is an element of a broadly distributed micronektonic fauna, much of which is cosmopolitan at low latitudes. Cephalopod abimdance in the upper 1,000 m was estimated at 50-70-10^ -km“^ on the basis of 4-mm mesh trawls. While this is an underestimate, particularly at either end of the micronektonic size spectrum (0.5-20 cm ML; see also Fig. 1), it probably is a better measure of the population than are our biomass values. Large individuals, while numerically a small fraction of the population, undoubt­ edly contribute much to total cephalopod biomass. These sizes are poorly sampled by our nets. For example, large Ommastrephes pteropus were frequently seen in surface waters around the ship at night, but the only specimens we obtained had jetted on deck. Abundance comparisons with other major micronektonic groups are attempted here, nevertheless, because comparative tows with nets of different mesh size seem to show escapement trends in cephalopods similar to those among midwater fishes (Gartner et al., 1989), penaeid shrimps (Flock, unpublished data) and heteropod molluscs (Rast, 1990). On the basis of Tucker trawl catches it appears that in the eastern Gulf micronektonic-sized cephalopods are more than an order of magnitude less abundant than micronektonic fishes (3.3-3.5 10*- km“^) and decapod shrimps (1.0-1.4- lO^-km”^) (Hopkins and Lancraft, 1984). Maynard et al. (1975) reported cephalopod abundances of 80-90-10^ -km“^ for waters off Hawaii and Clarke and Lu (1975), 150-180- 10^-km“^ for 18°N, 25°W in the northeast Atlantic. While regional variances occur, in part the result of differences in sampling protocol and gear, these estimates of cephalopod popu­ lations for low latitude oceanic areas do not differ all that widely. Cephalopods, then, though a common element of the micronekton, cannot be considered abun­ dant in oligotrophic systems relative to midwater fishes and shrimps. Their pop­ ulation size in fact is similar, at least in the eastern Gulf, to the other molluscan group of micronekton, the carinariid and pterotracheid heteropods (59 -10^ - km“^; Rast, 1990). Vertical distribution analyses reveal that all but three species occur in the epipelagic zone at night (Table 1). The three exceptions, Vampyroteuthis infernalis, Bathyteuthis abyssicola and Joubiniteuthis portieri primarily are known to inhabit deep (>500 m) water (Clarke and Lu, 1974, 1975; Roper and Yoimg, 1975), and they occurred in our collections only from tows that fished below 400 m. Indi­ viduals ofB. abyssicola and J. portieri, however, occasionally have been taken in the epipelagic zone at night in the North Atlantic (Clarke and Lu, 1974; Lu and Clarke, 1975). While distributions of the micronektonic cephalopod assemblage in the eastern Gulf are shallow at night for most species, sampling effort is a factor. The epipelagic zone was sampled much less frequently during the daylight hours than at night, with the ratio of volume filtered nearly 5 to 1 in favor of nighttime sampling. In the northeast Atlantic, where daytime sampling greatly exceeded ours (Clarke and Lu, 1974, 1975; Lu and Clarke, 1975), 22 of the species also recorded in our study occurred at less than 200 m during the day, whereas only 8 of these species were taken in this zone during the day in the eastern Gulf. Despite uneven sampling effort, diel vertical migration is suggested for at least some of the eastern Gulf species, especially among those in Table 1 listed from Mastigoteuthis sp. through Ornithoteuthis antillarum. Diel migration has, in fact, been reported by other authors for many of the species that occur in the eastem Gulf (Clarke, 1969; Clarke and Lu, 1974, 1975; Lu and Clarke, 1975; Roper and Young, 1975). Concentration of cephalopods in the epipelagic zone at night coincides with that of the other principal migrating groups (e.g., midwater fishes and shrimps). During the day, however, most cephalopods appear to remain in the upper 400

DWH-AR0127448 654 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991 m (Fig. 3) and thus are shallower than the bulk of the midwater fish and shrimp population (Heffeman and Hopkins, 1981; Hopkins and Lancraft, 1984; Gartner et al., 1987; Hopkins et al., 1989; Flock, 1989). Daytime cephalopod distribution in the eastem Gulf overlaps with juvenile stages of some of the “half-red”Sergestes (Flock, 1989) and caridean (Hopkins et al., 1989) species, a few weak or non­ migrating midwater fish species (Hopkins and Baird, 1981, 1985) and with mi­ cronektonic heteropods (Rast, 1990). All of the species found in the upper 400 m during the day show cryptic adaptations for survival in sunlit waters. The shallow dwelling sergestids (e.g., S. atlanticus, S. cornutus, S. pectinatus, S. vigilax) and carideans (e.g., juvenile Systellaspis debilis) have variegated pigment patterns and semi-transparent abdomens (Foxton, 1970; Herring, 1976) as well as coun- terilluminating photophores (Herring, 1976, 1985; Warner et al., 1979). Shallow mesopelagic fishes, e.g., Valenciennellus tripunctulatus and Argyropelectis hemi- gymnus, show considerable transparency, are capable of diel variation of their pigment pattem (Badcock, 1969) and also are well equipped with ventral pho­ t o p h o r e s for counterillumination (Denton et al., 1972; Case et al., 1977). Het­ eropods are largely transparent and species of Pterotrachea have iridophores in their epidermis and around the visceral nuclei which provide cryptic light patterns (Seapy and Young, 1986; Lalli and Gilmer, 1989). Cephalopods are similarly characterized by transparency, versatile chromatophores and an array of photo­ phores for counterilluminating (Young and Roper, 1977; Young and Mencher, 1980; Young, 1983). These attributes, along with excellent visual and swimming capabilities for avoidance of predators, equip cephalopods for survival in the shallow mesopelagic zone during the day. Vertical distance to the food-rich epi­ pelagic zone is much shorter than for deeper micronekton; presumably this would have significant energetic advantages.

Trophic Ecology.—0\xr diet analyses indicate that the cephalopods captured by our gear are primarily crustacean feeders, with copepods the major prey (Fig. 7). Euphausiids also are common food items and probably are important in terms of caloric value, given their larger size. Larger cephalopods (> 4 cm ML) are more piscivorous, a fact reported by many authors (Karpov and Cailliet, 1979; Roper et al., 1984; Lipinski, 1987). The low food incidence in cranchiids stands out among the micronektonic cephalopods. Cranchiids have a less firm musculature than most other teuthoids, hence a less active life strategy would be predicted. A lower activity level would be characterized by a reduced metabolic rate and lower caloric demands, which would be reflected in the infrequent feeding of cranchiids implied by our data. A comparison of the diet of cephalopods with that of other micronekton groups and with the composition of plankton is presented in Table 5. Cephalopod diet composition in its general aspect is similar to the composition of co-occurring zooplankton, though within-group selectivity, e.g., strong positive selection for euphausiids and for the genus Pleuromamma among copepods, is apparent. Co­ pepods are the numerically prevalent cephalopod food, similar to that of the micronektonic fishes and shrimps. Reliance on copepods, however, appears to be greater in cephalopods than in the other two groups. Feeding patterns in cepha­ lopods contrast sharply with their molluscan relatives, the heteropods, in that in the eastem Gulf the latter feed mostly on gelatinous prey (Rast, 1990). Cluster anlaysis reveals a degree of inter- and intraspecific resource partitioning among the most abundant species (Fig. 5). This is a function of ontogenetic shifts in diet as well as of individual species preferences. Intracluster variations, on the other hand, appear to be minimal. This was noted as well by Hayward and

DWH-ARO 127449 PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 655

<2 cm ML 2-4 cm ML >4 cm M 1 0 0

80 CO

LU

60 yj Q

40 V’v:;;

LU o cc LU vV:;>;vv/vvV*'? 20

CO CO 9 Q 0 O 0 1 Q. 1 I- O I- =3 I— 3 3 O LU o LU LU

KEY: ^ COPEPODS H I EUPHAUSIIDS

E m OTHER INVERTEBRATES [ZH FISH Figure 7. Summary of the diet composition of micronektonic cephalopods from the eastem Gulf of Mexico.

DWH-AR0127450 656 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Table 5. Percentage composition of diets of principal groups of micronekton and of plankton numbers occurring in the epipelagic zone at night in the eastem Gulf of Mexico. Fish include numerical dominants: 25 species of myctophids (Hopkins and Gartner, unpublished data), an abundant gon- ostomatid (Lancraft et al., 1988) and one stemoptychid species (Hopkins and Baird, 1985); shrimps include the seven dominant species of sergestids (Flock, 1989) plus the two shallow occurringGennadas species (Heffeman and Hopkins, 1981); heteropods are represented by four of six micronektonic species found in the Gulf (Rast, 1990); plankton information is from Hopkins (1982 and unpublished data)

Mid water Penaeid Heteropod fishes shrim ps molluscs Cei^alopods Plankton Copepods 58 57 23 83 84 Euphausiids 12 6 13 10 <1 Ostracods 10 15 1 1 3 Pleuromamma spp. 24 9 <1 62 2 Total crustaceans 87 79 37 95 87 Total non-crustaceans 13 21 63 5 13

McGowan (1979) for spatially co-occurring species of copepods in the north central Pacific and by Hopkins (1985) for closely related Southern Ocean copepods in the same feeding guild. Competition in any case may derive more from other micronektonic taxa such as midwater fishes and shrimps as these groups might be at least an order of magnitude more abundant than cephalopods. In the eastem Gulf the entire cephalopod assemblage is much less abundant thtm any single dominant species of midwater fish or shrimp (Heffeman and Hopkins, 1981; Gartner et al., 1987; Flock, 1989). Selection for P/ewromamma copepods is strong, particularly among cluster IV teuthoids (Table 4). This prey occurs in relatively high percentages in diets of midwater fishes and shrimps as well. The Metridiidae in general and Pleuromamma in particular are highly bioluminescent (David and Conover, 1961; Bames and Case, 1972; Latz et al., 1987; Bannister and Herring, 1989) and while certainly not unique to this family (Clarke et al., 1962; Herring, 1988), their particular display might make them especially vulnerable to predation (see review by Young, 1983). The three abundant species which forage heavily on Pleuromamma, i.e., Pterygioteuthis gemmata, P. giardi and Pyroteuthis mar­ garitifera, have diel vertical distributions in the eastem Gulf (Passarella, 1990; see also Roper and Yormg, 1975; Caims, 1976) that coincide with the migrations of all four species of Pleuromamma (Bennett and Hopkins, 1989), and the pro­ portion of Pleuromamma in their diets remains high (sample averages > 84%) regardless of time of capture. Day-night concurrence of predator and prey, along with the presumed ability through excellent vision to locate Pleuromamma throughout the diel cycle, might help explain the observed absence of strong periodicity in daily feeding. In summary, pelagic cephalopods in the eastem Gulf of Mexico constitute a taxonomically diverse group with pan-oceanic affinities. They are common but not abundant micronekton which are essentially cmstacean feeders when small, then they shift toward piscivory as they mature. Considering their moderate population size in oligotrophic systems, the role of cephalopods is perhaps less significant as predators on zooplankton than is their role at higher trophic levels where they are important predators on micronekton and nekton and are them­ selves food for these groups, and for seabirds and humans as well.

A cknowledgments

This paper is dedicated to the memory of Professor Gilbert L. Voss. Nancy Voss, his wife, was especially helpful in the systematics aspects of this study and her generous assistance is gratefully

DWH-ARO 127451 PASSARELLA AND HOPKINS: GULF CEPHALOPOD ASSEMBLAGE 657

appreciated. We would also like to thank C. Roper and M. Vecchione (Smithsonian Institution) for their careful review of the manuscript and for examining some of our cephalopod material. We appreciate as well the assistance o f T. Lancraft (U. So. Fla) in the early stages o f getting this manuscript together. This research was supported by National Science Foundation contracts DES 75-03845, OCE 75-03845 and OCE 84-10787.

L it e r a t u r e C it e d

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D a te A c c e p t e d : May 21, 1991.

A d d r esses : (K.C.P.) Johnson Engineering, Inc., 2158 Johnson St., Fort Meyers, Florida 33902; (T.L.H.) Department of Marine Science, University of South Florida, St. Petersburg, Florida 33701- 5016.

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