Cephalopoda: Octopodidae)

BULLETIN OF MARINE SCIENCE. 56(3): 752-766, 1995

DESCRIPTIVE ECOLOGY OF TWO SOUTH AMERICAN ELEDONIDS (CEPHALOPODA: OCTOPODIDAE)

J. Angel A. Perez and M. Haimovici

ABSTRACT Eledone massyae and Eledone gaucha are small octopods that coexist along the continental shelf and slope of southern Brazil. A comparative study of the population structure, distribution and diet of these species was carried out based on bottom trawl material from fishing surveys off Rio Cirande do Sui State (Brazil), between 30043'S and 33°45'S and the isobaths of 10 and I 10m. The two species occurred throughout the year in trawls deeper than 40 m, on both sandy and muddy bottoms of the outer continental shelf and upper slope. E. massyae and E, gaucha were found at bottom temperatures ranging from 10 to 22°C in tropical, subtropical and s'.lbantarctic waters. Young E. massyae appear on the continental shelf in late summer and feed predominantly on small crustaceans such as amphipods. A single cohort of maturing animals remains on the shelf during winter and spring, switching their diet to larger prey, such as portunid crabs and polychaetes. In late summer, males and females migrate to spawning grounds outside the study area. Juveniles of E. gaucha occur on the shelf mainly during summer and autumn. Males and females seem to mature on the shelf throughout the year, although no true cohorts could be defined. In all size e1asses, small benthic crustaceans, such as amphipods and isopods are the predominant food items. There is no evidence of habitat segregation between these two eledonids, but as adults, they seem to exploit different food resources,

Cold-water octopods constitute over half of the total number of benthic Octo- poda species reported from the southern Brazilian coast (Haimovici and Perez, ]99] b). These species are commonly found over soft bottoms of the continental shelf and slope, and their northern distribution is associated with the influence of cold waters of the MalvinaslFalkland Current on the central continental shelf (Palacio, 1977; Haimovici et aI., 1989; Haimovici and Perez, 199Ib). Among the most abundant, two congeneric species, Eledone massyae Voss 1964 and E. gaucha Haimovici 1988, coexist on the outer shelf and slope between Cabo Frio (Lat. 23°S) and Chui (Lat. 34°S) (Haimovici, 1985; Haimovici and Andriguetto, 1986; Haimovici, 1988; Haimovici et aI., 1989; Perez and Haimovici, 1991b). E. massyae occurs seasonally on the Rio de Janeiro continental shelf (Costa and Fer- nandes, 1993) where it forms part of the octopod landings in the trawl fishery (Costa and Haimovici, 1990). Its distribution extends southward to Peninsula Val- dez (Lat. 43°S), Argentina (Voss, 1964). Morphologically similar, but smaller in size, E. gaucha has been recently differentiated from E. massyae (Haimovici, 1988; Levy et aI., 1988). The review of several cephalopod collections indicated that the species, formerly misidentified as E. massyae, occurs along the southern Brazilian coast (Perez and Haimovici, 1991a), and has not been recorded south of Brazilian waters. A series of groundfish surveys conducted off the coast of the Rio Grande do SuI State between 1981 and 1987 collected both species on the central continental shelf out to 600 m depth (Haimovici and Andriguetto, 1986; Haimovici and Perez, 1991a). Preserved samples from these surveys have provided information for comparative studies on the reproductive biology of both species in the area (Perez et aI., 1990; Perez and I-Iaimovici, 1991b; Perez et aI., in press). This paper describes the habitat and presents comparative data on the diets and distribution of E. massyae and E. gaucha on the southern Brazilian coast.

752 PEREZAND"!A1MOV1Cl:ELEDONIDOCTOPODECOLOGY 753

Rio Grande do Sui : 30 Brazil

100 km

• detrit. sandy transit. slope

Figure I. Study area. Bottom type distribution according to Martins et al. (1972) is indicated. The an'ow indicates the location of the survey area in the southwest Atlantic Ocean. detrit., banks of shell debris; sandy, sandy bottom type; transit., transitional bottom typc consisted of a mixture of sand and mud; slope, slope bottom type consisted of mud.

MATERIAL AND METHODS

The material was obtained from 16 groundfish surveys of the RN ATLANTICOSULof the Rio Grande University (Brazil), from 1980 to 1985. The cruises occurred throughout the year and covered the southern Brazilian continental shelf between Solidao (30043'S) and Chuf (33°45'S) at depths ranging from 10 to 160 m (Fig. I). A bottom trawl net with a 52.9 m footrope, 31.3 m headrope and a 50 mm stretch-mesh cod end was used to collect the samples. The trawl hauls were done at 3 kn for 30 to 60 min, between dawn and dusk. The specimens of E. massyae and E. gaucha were separated from the total catch, weighed to the nearest O. I g, the dorsal mantle length (ML) measured in millimeters, and then fixed in 10% buffered 754 BULLETIN OF MARINE SCIENCE. VOL. 56, NO.3. 1995

Table 1. The percentage distribution of tows per depth stratum, bottom type and subarea in the four seasonal cruises considered for analysis of the distribution of E. massyae and E. gaucha

No. Depth stratum (Ill) Bottom substrate Subarea of Survey tows. Bottom temp. 0-20 20-40 40-60 60-80 >80 Sandy Trans. Slope North South

Summer 42 12.8-22.9 30.9 9.5 23.8 19.0 16.7 61.9 26.2 11.9 35.7 64.3 Autumn 41 15.5-22.6 19.5 21.9 24.4 17.1 l7.1 58.5 29.3 12.2 36.6 63.4 Winter 54 11.3-17.8 16.7 11.1 22.2 24.1 25.9 44.4 31.5 24.1 46.3 53.7 Spring 34 12.6-20.2 20.6 14.7 17.6 20.6 26.5 44.1 29.4 26.5 55.9 44.1 Total 171 11.3-22.9 21.6 14.0 22.2 20.5 21.6 52.0 29.2 18.7 43.3 56.7

formalin. In the laboratory, the specimens were transferred to 70% ethanol, and their reproductive organs and digestive tracts were dissected for reproductive studies (Perez et aI., 1990; Perez and Haimovici, 1991b; P,~rez et aI., in press) and diet analysis. The population size structurc and sex ratio was analyzed for 294 specimens of E. massyae, and 169 specimens of E. gaucha collected in all 16 cruises combined. An additional 126 E. massyae and 13 E. gaucha. obtained from the commercial groundfish fishery, were included in the diet analysis. The contents of the crop and the stomach werc examined under a dissecting microscope, and the food items identified to the lowest taxonomic level possible and expressed by their frequency of occurrence. The patterns of distribution of E. massyae and E. gaucha, were studied in 171 tows of four selected cruises made during 1982 and 1983 (Table I). Due to the frequent occurrence of Eledone spp. entangled in the wings of the trawling nets (Haimovici, 1988), the gear was not considered a reliable estimator of abundance and only the frequency of occurrence of the species per tow was used in the analysis of distribution. The cnlises were classified as: summer, January 1982 (cruise 1/82); autumn, April 1983 (cruise 4/83); winter, September 1983 (cruise 9/83) and spring, November 1983 (cruise 13/83). The study area was divided into subarea North (between 30046'S and 32°30'S) and subarea South (between 32°30'S and 34°20'S) (Fig. I), and six depth strata with boundaries at 20, 40, 60, 80 and 100 m were defll1ed. The boltom type was estimated by plotting the tows on a chart of the sediment distribution of southern Brazil (Martins et aI., 1972). The bottom sediments were classified into three main zones: sandy, transitional, and slope. The relationship between the frequencies of occurrence of the two species and the distribution of tows per season, subareas, depth strata and bottom types (Table I), was tested using the Chi-square statistic with a confidence level of 0.05. The coexistence of E. massyae and E. gaucha was assessed by the frequency of tows where both species occurred in relation to the total number of tows with the presence of at least one species. The water masses were classified according to Castello and Moller (1977) from the bottom temperature and salinity data obtained after each tow.

RESULTS Physical Environment.-The southern Brazilian continental shelf is 125 km wide on average, breaking between the 150 and 185 m isobaths. It reaches its maximum width (180 km) south of Rio Grande (Lat. 33°S) and narrows towards the north (Fig. 1). The bottom of the inner shelf is characterized by a sandy zone that extends down to 1he 50 m isobath. Along this zone, banks of shell debris occur parallel to the coast. Mud rich in silts and clays predominates on the outer shelf and slope between the 100 and 3,000 m depth (slope zone). The transitional zone of variable proportions of sand and mud separates the inner sandy zone from the outer slope zone (Fig. 1). Rocky bottoms occur on the slope, predominantly in submarine canyons. The oceanographic conditions of the southern Brazilian coast are determined by the seasonal influences of four water masses: a. Subantarctic water (with temperatures between 4.5 to 16SC and salinities between 33.5 and 34.2%0) is derived from a coastal branch of the Malvinas/Falkland Current, and flows northward reaching its northernmost penetration to around 31-32°S during the winter. b. Tropical water is derived from the Brazil Current (with temperatures between 18 to 25.5°C and salinities between 36 to 36.9%0), and flows southward reaching its southernmost penetration during the summer. c. Subtropical water flows northward PEREZ AND HAIMOVICI: ELEDONID oerOPOD ECOLOGY 755

and results from the mixing of the Subantarctic and Tropical water masses. d. Coastal water occurs permanently over the inner shelf and is characterized by low salinities due to the freshwater runoff from the Rio de La Plata. In the four cruises considered for distribution analysis, the bottom temperature ranged from 11.3 to 22.9°C (Table 1). Maximum bottom temperatures occurred in coastal waters and decreased towards the shelf break. Cold waters originating from the subantarctic water mass, and from the mixing between subantarctic and coastal waters, were predominant during the winter cruise (Fig. 2C). During the spring and summer cruises in the southern subarea, cold-water cores (temperature <16°C) originating from the influence of the subantarctic waters occurred at 40- 80 m depths (Fig. 2A, D). In the autumn, high temperatures dominated the continental shelf (Fig. 2B). The benthic habitat on the middle continental shelf between 40 and 80 m depth was exposed to temperature fluctuations as wide as 10°C over the year. Distribution.-Neither species occurred in the shallowest depth stratum and the frequency of occurrence of E. massyae increased at deeper strata (Fig. 3b). E. massyae was more frequent in the spring tows and on the slope bottom types (Fig. 3a, c). E. gaucha occurred predominantly in the autumn and on the transitional bottom types (Fig. 3a, c). It was less frequently caught in the northern subarea (Fig. 3d). The frequency of occurrence of both species was significantly associated with the different bottom types. Depth stratum and subarea effects were also significant in E. massyae and E. gaucha respectively (Table 2). In a total of 60 tows in which at least one of the species occun'ed, both species co-occurred in 38.3% (significant p = 0.075). The coexistence of both species was significantly associated with the subarea (Fig. 4d, Table 2) due to the low occurrence of E. gaucha in the northern subarea. The range of temperatures and salinities for tows with an occurrence of either E. massyae or E. gaucha is presented in Table 3. Eledone spp. occurred predominantly under the influence of tropical, subtropical and subantarctic waters. In the spring and summer cruises neither species occurred at the higher temperatures, and both were found associated with the cold cores around 60 ill deep in the southern subarea (Fig. 2A, D). In the autumn cruise, both species were caught at the maximum temperatures (21.soC) on the shelf (Fig. 2B). In the winter cruise, Eledone spp. were found across the temperature gradient on the central shelf and under the influence of subantarctic cold waters in the southern subarea (Fig. 2C).

Population Size Structure and Sex Ratio.-Minimum and maximum sizes of E. massyae were caught during the summer cruises on the central shelf. Females and males ranged from 24 to 91 mm ML and 22 to 80 mm ML respectively. E. gaucha attained smaller sizes, ranging from 14 mm ML in both sexes to 55 and 47 mm ML, for females and males respectively. The frequency distributions of ML classes per season and depth strata of the two species are shown in Figures 5 and 6. In E. massyae, more than one cohort is present during the summer months. Young octopods occurred in the shallower depth stratum and formed a modal ML group that increased progressively in subsequent seasons. The cohort formed by the largest individuals seems to dis- appear from the study area after the summer (Fig. 5A). A less conspicuous single cohort of E. gaucha seems to be present throughout the year (Fig. 5B). The proportion of males and females observed for E. massyae (1 male: 2.3 females) differed significantly from the 1:1 ratio except in spring, and at depths greater than 100 m (Table 4). In general, females were more numerous than males. 756 BULLETIN OF MARINE SCIENCE. VOL. 56. NO.3. 1995

5a 52 50 53 52

A. Summer B. Autumn 31 ~JI: 32 ~~ \ 32

•• 34

C. Winter D. Spring

33 33

34 34 ~:.~...

53 52 51 50 53 52 51 50

• E.mass)'ae 1!{ E.gaucha o both spp. • neither spp.

Figure 2. The occurrence of E. massyae and E. gaucha and bottom isotherms on four seasonal surveys off southern Brazil. PEREZ AND HAIMOVICI: ELEDONID OCTOPOD ECOLOGY 757 a 34 40 41

30 S4 42 II! 20

0 summer autumn winter spring b 60 35 37 50

40 38

II! 30

20 24

10 37 n. 0 <20m 21-40m41-60m61-80m >80m

Figure 3. The frequency of occurrence of E. massyae (solid bars) and E. gaucha (open bars) in the total number of tows (indicated above each class) by: a. seasons, b. depth strata, c. bottom types, d. subareas.

Between 60 and 80 m around four females were caught for each male. The sex ratio was significantly associated with depth stratum. In E. gaucha, the ratio 1:1 was found to be significant except in the winter cruises and at depths between 60 and 80 m, where females predominated (Table 4). Neither the seasons, nor the depth strata significantly affected the sex ratio. Food and Feeding.-Food remains in the digestive tracts were found in a total of 109 of the 326 E. massyae examined, and in 135 of the 182 E. gaucha examined. The main food items present in the diets of E. massyae and E. gaucha were identified through a variety of rigid fragments found in the stomach and crop contents. In E. gaucha, the prey items were small and little damaged. Therefore more detailed classification of prey taxa was possible for this species (Table 5).

Table 2. Analysis of the effect of the frequency of tows per season, depth stratum, bottom type and subarea in the frequency of occurrence of Eledone spp. Chi-square values (X2) and degrees of freedom (OF) for the analysis are given. Asterisks indicate significant relationship between the frequency of the factors on the Eledone spp. occurrence (Ot = 0.05). For the analysis of the co-occurrence of both species in the same tows, frequency of occurrence of tows in which both species were caught is calculated from the total number of tows in which at least one species occurred.

E. massyae E. galicha Co-occurrence x' DF x' DF x' DF Season 4.178 3 6.60 3 1.42 3 Depth strata 27.115* 3 5.25 3 1.01 2 Bottom type 28.62* 2 7.37* 2 5.15 2 Subarea 1.3215 1 13.15* 1 6.19* I 758 BULLETIN OF MARINE SCIENCE, VOL. 56, NO.3, 1995

C 60 a 60 23 10 SO SO

40 40

30 * 30 * 20 20

10 10

0 0 summer autumn winter spriog sandy trans. slope b 60 d 3S 40 18 30 SO 2j 40 20 30 oj! * IS 20 10

0 0 <20m 21-4·Jm 41-60m ol·8Om > 80m nonh south Figure 4. The frequency of occurrence of tows with the presence of both E. massyae and E. gaucha in the total number of tows in which at least one species was caught (indicated above each class) by: a. seasons, b. depth strata, c. bottom types, d. subareas.

In E. massyae, most of the prey items found were not identified by their external body fragments but by internal structures due to damage during predation. In addition, a large proportion of the remains in E. massyae consisted of fleshy material that could not be identified at any level. The results indicate that the prey found in E. massyae were probably larger than that in E. gaucha. Crustaceans were the most frequent items found in the digestive system of both species (Table 5)" and were divided into two general categories: (a) microcrustaceans, including benthic: amphipods (orders Gammaridea and Caprellidea) and isopods identified by carapace fragments and appendages; and (b) macrocrustaceans, including d.ecapods of the Orders Brachiura and Anomura, identified mainly by internal structures such as phyllobranchiate gills and chitinous teeth of the stomach gastric mills. In E. massyae, macrocrustaceans and particularly portunid crabs, were the predominant food items, occurring with increasing frequency in larger animals (Fig. 7a). In E. gaucha of all size classes, microcrustaceans dominated (Fig. 7b). Polychaetes were the second most frequent item in both species (Table 5) and were identified by the presence of setae and mandibles in the stomach and crop remains. Other food items included bony fishes and molluscs. In two specimens of E. massyae fragments of Eledone sp. arms were found.

DISCUSSION Octopods of the genus Eledone have been reported from the tropical and warm- temperate waters of the Atlantic and Pacific Oceans (Voss, 1988). In the North Sea and in the Mediterranean, E. cirrhosa and E. moschata normally occur at temperatures below 16°C. This temperature was considered to be a boundary for PEREZ AND HAIMOVICI: ELEDONID OCTOPOD ECOLOGY 759

Tab]e 3. Minimum, mean and maximum values of temperature cae), salinity (%0) and depth (m) for the tows with occurrences of E. massyae and E. gaucha

E. [:llucha E. massyae Summer No. of tows 5 10 Bottom temp. 13.3-16.2-18.2 12.8-15.8-18.2 Salinity 34.25-35.19-35.96 29.95-34.41-36.08 Depth 56-65.2-91 56-77 .5-36.08 Autumn No. of tows 14 9 Bottom temp. 17.3-19.7-21.5 17.3-19.2-21.0 Salinity 31.1-33.87-35.4 32.40-34.39-35.80 Depth 30-66.6-100 44-76.7-100 Winter No. of tows 11 14 Bottom temp. 11.3-]2.3-14.1 11.3-15.2-18.6 Salinity 25.9-33.05-35.87 27.77-33.87-36.05 Depth 22-72-140 44-89.5-140 Spring No. of tows 6 14 Bottom temp. 15.4-16.37-17.8 ]5.4-16.5-18.0 Salinity 31.38-34.05-35.70 31.4]-35.08-35.86 Depth 55-8].5-100 35-80.2-]00 Total No. of tows 36 47 Bottom temp. 11.3-16.4-21.5 11.3-16.5-21.0 Salinity 25.98-33.83-35.96 27.77-34.43-36.00 Depth 22-70.5-140 35-81.7-]40

the distribution of E. cirrhosa at lower latitudes in the Atlantic Ocean (Boyle, 1983). In the southwest Atlantic, the distributions of E. massyae and other cold- water species in tropical waters, have been attributed to their tolerance for higher temperatures (Palacio, 1977). In southern Brazil, our results show that E. massyae and E. gaucha can occur in tropical waters at temperatures as high as 21.8°C. In spring and summer, however, temperatures higher than 18°C that predominate on the inner shelf were generally avoided, and both species were associated with the colder subtropical and subantarctic waters of the central shelf. Although it seems that the South American Eledone spp. indeed tolerate high temperatures, their distribution seems to be associated with the influence of subantarctic waters that occur along the whole range of their distribution in the southwest Atlantic (Hai- movici and Perez, 1991a). This association is also supported by the occurrence of E. massyae on the shelf on the northern coast of Rio de Janeiro state (Lat. 23°S) during spring and summer, coincident with a seasonal upwelling of subantarctic waters (Costa and Fernandes, 1993). The interpretation of the distribution patterns of E. massyae and E. gaucha in our study area is affected by the dubious sampling efficiency of the trawl used. The ability to escape from the trawl net as it is being hauled has been observed for young E. cirrhosa in the North Sea (Boyle and Knobloch, 1982). Similarly, small Eledone and particularly E. gaucha, were frequently found entangled in the wings of the net instead of in the cod end (Haimovici, 1988). This suggests that their vulnerability to the trawl net is limited, especially in the case of deep tows 760 BULLETIN OF MARINE SCIENCE, VOL. 56, NO.3, 1995

A SUMMER B SUMMER 20 N~71 40 N~43 16

30 12 '" '" 20

0 0 10 20 30 4

AUTUMN AUTUMN 35 25 NE35 30 N=28 20 25

20 15 "' '" '" 10 10

0 10 20 30 4

WINTER WINTER 25 1'1-93 20

'" ]0

.. ., .. .. 70 .. ]0 20 30 40 50 60 70 " MANTLE LENGn!" mm MANTI..E LBNGTII mrn

SPRING SPRING 25 30 1'1-113 1'1-24 2.\ 20

20 IS 15 '" 10 '" ]0

0 10 10 20 30 40 SO 60 70 MANTLE LENGnI mm

Figure 5. Seasonal frequency distributions of mantle length classes (mm). A, E, massyae, B. E. gaucha.

when the net is hauled up for long periods of time. The low occurrence of small octopods in deep tows, therefore, was regarded with caution. E. massyae and E. gaucha were consistently scarce on the sandy bottoms of the inner shelf and were found, throughout the year, on the central and outer shelf PEREZ AND HAIMOVICI: ELEDONID OCTOPOD ECOLOGY 761

A < 60m B < 60 nt 20 25

16 20

20 ~ ~ 50 ~ 70 W W 100 10 20 ,0 4ll 50 60 10 MANTLE LENGTIl mm MANTLE LENGTH mm

60 - 80 nt 60 - 80 m 20 ,0

16 25

20 12 If' 15

o 10 10 20 30 40 50 60 70 MANTI..E LENGTII mm

80 - 100 m 80-100 m ,0 25

25 20

20 15 If' 15 10 10

o 10 90 100 10 70

> 100 m > 100 nt 60

16 N •••.l0 .<0

12 40

If' ,0

o 10 W m ~ m 60 M W ~ ~ 10 60 10 MANTLE LENGTH mm

Figure 6. Frequency distributions of mantle length classes (mm) by depth strata. A. E. massyae, B. E. gaucha.

where clay and silt sediments dominate. The significant increase in the frequency of occurrence of E. massyae at greater depths suggests that the study area rep- resents the upper limit of the species bathymetric distribution. E. gaucha was also scarce on the slope sediments and in the northern subarea. These results, however, 762 BULLETIN OF MARINE SCIENCE, VOL. 56, NO.3, 1995

Table 4. Analysis of the sex ratio of E. massyae and E. gaucha. Number of males and females and Chi-square values p'~r seasons and depth strata are given. Asterisks indicate significant ratios COt = 0.05). Xd, is the Chi··square value calculated from the analysis of the effect of seasons and depth strata on the sex ratios.

E. maSj'yae E. gaucha x' x' N Males Females \:\ Xd N Males Females ):1 Xd

Seasons Summer 7] 19 52 7.2] 43 ]6 27 2.32* Autumn 33 7 26 9.82 41 21 20 0.00* Winter 78 23 55 12.32 65 24 41 3.94 Spring 112 45 67 1.28* 6.32 20 II 9 0.05* 3.87 Depth strata <60 m 53 IS 38 9.]3 98 43 55 ].47* 60-80 m 78 15 63 28.32 24 7 17 4,17 80-100 m 103 38 65 6.56 30 15 ]5 0.00* >100 60 26 34 0.82* 9.80* 17 7 10 0.53* 2.52 Total 294 94 200 37.5 169 72 97 3.41 * may reflect the sampling limitations of deep tows, because slope sediments are dominant at greater depths and deep tows were more frequent in the North subarea, where the shelf is narrower. In most cases, however, the distribution of both species overlapped significantly. If the sampling limitations are considered, then there was no evidence of macrohabitat segregation between the two species in the study area. The life cycle of E. massyae proposed by Perez and Haimovici (1991 b) esti- mates a life span of approximately two years. Females die after the single spawning event that occurs in the autumn outside of the area studied. Juveniles appear on the shelf during the following summer, where they grow, mate and reach advanced stages of sexual maturity by the spring and summer of their second year. The size structure variation of this species on the shelf indicates that recruits appear on the cenltral continental shelf during the late spring/summer months when members of the previous years' cohort are still present. In the subsequent months, the cohort formed by octopods in their first year grows on the shelf attaining their maximum sizes the following summer. The search for rocky bottoms suitable for spawning seems to be a plausible explanation for the disappearance of the adult cohort from the study area in the autumn. Inshore and offshore migrations proposed for E. cirrhosa. in the Catalonian Sea (Mangold-Wirz, 1963; Moriyasu, 1984) and in the Tyrrhenian Sea (Wurtz et aI., 1992) respectively, were related to the availability of rocky bottoms in the area. Because E. massyae was never found associated with banks of shell debris and because rocky bottoms are scarce on the continental shelf (Fig. 1), an offshore spawning migration as suggested by Perez and Haimovici (1991b) is supported. A similar migratory pattern has also been reported in Rio de Janeiro waters (Costa and Fernandes, 1993). Variable maturity stages of males and females E. gaucha occur throughout the year on the shelf with no distinct seasonal pattern (Perez et aI., in press). It is likely that more than one cohort coexists on the shelf but, because recruits were poorly represented in the samples, this distinction through the analysis of size structure was not possible. In E. massyae, the unbalanced sex ratio seems to reflect a bathymetric segregation of sexes as reported for E. cirrhosa in the Mediterranean (Mangold-Wirz, 1963; Palumbo and Wurtz, 1983; Moriyasu, 1983). Sex ratios close to 1:1 at PEREZ AND HAIMOVICI, ELEDONID OCTOPOD ECOLOGY 763

Table 5. List of food items identified in the stomach and crop contents of E. massyae and E. gaucha (percentages express the frequency of occurrence of the food categories in the total number of digestive tracts examined per species)

E. ;:aucha E. maSSYlle

Freq. % Freq. % TOlal: 135 100 109 100

Teleostei I 0.7 6 5.5 Crustacea \33 98.5 78 7\.6 Amphipoda 109 80.7 7 6.4 Caprellidea 13 9.6 Prolomina sp. 3 2.2 Unidentified 10 7.4 Gammaridea 96 71.1 Proboloides sp. I 0.7 Slenolhoe sp. I 0.7 Amphylochun napolilanus I 0.7 Gamaropsis sp. 3 2.2 Gamaropsis lompsoni 3 2.2 Gamaropsis logoensis I 0.7 Pseudogamphobus barnardi 2 \.5 Paramelo pella sp. 2 1.5 Ampeliscypholes sp. I 0.7 Unidentified 81 60 lsopoda 35 25.9 Brachyura 7 5.1 33 30.3 Panopeus sp. I 0.7 Portunus sp. 1 0.7 12 I] Casmocarcinus lipicus I 0.7 Unidentified 4 3 21 ]9.3 Anomura 7 6.4 Munida sp. 7 6.4 Stomatopoda 1 0.7 Unidentified 52 38.5 ]9 17.4 Mollusca 10 9.2 Gastropoda 6 5.5 Cephalopoda 4 3.7 Eledone sp. 2 1.8 Polychaeta 25 18.5 20 18.3 Siga10nidae ]5 11.1 15 13.8 Unidentified 10 7.4 5 4.5 Unidentified 2 \.5 30 27.5

depths around 100 m and during the spring months when the peak in mating activity has been estimated to occur (Perez and Haimovici, 1991b). Alternatively, the underestimation of the normally smaller males by the trawl net may also have contributed to the unbalanced representation of sexes in the samples (Boyle and Knobloch, 1982; Boyle, 1986; Boyle et ai., 1988). In this case, however, a significant superiority in the number of females over males would also have been expected for E. gaucha, since sexual dimorphism has also been observed in this species (Haimovici, 1988 and our data). The analysis of the stomach and crop remains indicates a distinction between the feeding habits of E. massyae and E. gaucha. As E. massyae grows on the continental shelf, it changes its diet from epibenthic isopods, amphipods and polychaetes to larger prey such as crabs. E. gaucha, of all size classes available in this study, captures and ingests whole small preys, mainly epibenthic amphipods and isopods. Therefore, it is suggested that, at least during adult life, E. massyae 764 BULLETIN OF MARINE SCIENCE, VOL. 56. NO.3. 1995

a 70 b 100

60 80 50

40 60

3D 40 20 to

<40mm 40-50 rom 50·60 rom >60mm MLcJ.ass

[0 polich. _ macroc. ~ microc. 0 olhcrs I

Figure 7. The freqUt~ncyof occurrence of the main prey categories in the stomach and crop remains of a. E. massyae and b. E. gaucha. polych., polychaetes; macroc., macrocrustaceans; microc., microcrustaceans; others, include bony fishes and molluscs.

and E. gaucha coexist on the continental shelf of southern Brazil by exploring different food resources. The preference for crustaceans and particularly crabs has been reported for E. cirrhosa (Sanchez, 198 I; Moriyasu, 1981; Boyle and Knobloch, 1981) and other octopodids (for review see Mangold, 1983b). Epibenthic amphipods and isopods are occasional octopodid prey (Boletzky and Hanlon, 1983; Nixon, 1987), frequently reported for cold-water forms such as Bathypolypus arcticus (O'Dor and MacAlaster, 1983) and cirrate octopods (Villanueva and Guerra, 1991). Surveys of crustacean fauna and groundfish trophic relations have shown that portunid crabs and epibel11thicamphipods are relatively abundant on the southern Brazil continental shelf (Tommasi et aI., 1973; Bordin, 1987; Ribeiro, 1982). Therefore E. massyae and E. gaucha appear to feed predominantly on easily available prey throughout their life on the continental shelf.

ACKNOWLEDGMENTS

We thank F. D'Incao, R. Capitoli and Y. Wakabara for the identification of the crustacean food items. J. H. Muelbert, 1. Barriga and J. Hoar critically read the manuscript. The first author was supported by a scholarship of the Ministry of Education of Brazil (CAPES).

LITERA TURE CITED

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DATE ACCEPTED: December 28, 1993.

ADDRESSES: (.f.A.A.P.) Biology Department, Dalhousie University, Halifax. Nova Scotia, B3H 4Jl, Canada; (M.H.) Departamento de Oceanografia, Fund. Universidade do Rio Grande, ex. Postal 474, Rio Grande, RS, 96 500-900, Brazil.