Benthos Biomass and Oxygen Deficiency in the Upwelling System Off Pem

/our1lll1 01 Marine Research, 41, 263·279, 1983

Benthos biomass and oxygen deficiency in the upwelling system off Pem

by Rotger Rosenbergl, Wolf E. Amtz2, Esmeralda Cbuman de Flores2, Luis A. Flores2, Guido Carbajal2, Imme Finger2 and J. Tarazona8

ABSTRACT Data are presented on macrobenthic (;;:: 1 mm) biomass and species composition, sulfur bacteria (Thioploca), demersal fish catches, organic content of sediment and dissolved oxygen at 65 stations (35-360 m) along the upwelling area off north Peru in 1980-1981. Oxygen concentration close to the bottom was high only down to about 20 m depth and at 20-700 m it was generally < 0.8 mil-I. Organic content of sediment increased significantly with water depth. Macrofauna were found at all stations with a general dominance of small polychaetes. Macro- faunal biomass showed a significant positive correlation with oxygen concentration; below 0.6 ml 1-1 of oxygen biomass was impoverished. No correlation was found between biomass and depth. A mean macrofaunal biomass of 5.9 g 0.1 m-l was recorded at depths < 100 m and 3.1 g 0.1 m-ll at 100-200 m. Biomass was higher in the north compared with the south and showed a significant positive correlation with demersal fish catches. In contrast, Thioploca biomass showed a significant negative correlation both with macrobenthic biomass and demersal fish catches. From this study and previous work, we conclude that oxygen concentration was the dominant ecological factor determining macrobenthic biomass and species composition in the upwelling area off Peru and northern Chile. The benthic fauna living in low oxygen concentrations have probably developed this tolerance through evolutionary adaptation. Based on oxygen concentration and exposure, five zones in this upwelling area are characterized and their dominant benthic macrofauna documented.

1. Introduction The coastal upwelling zone off the coast of Peru (Fig. 1) and northern Chile (4-23S), stimulates high phytoplankton production within 100 km of the coast.. This production results in the world's largest fish catches which peaked in 1970 with landings exceeding 12 million metric tons of anchovy (Engraulis ringens). Sub- sequent to 1971 catches have declined considerably, and in 1977-1981 approximately 1 million tons were landed. Anchovy and sardine, the fish species of great~t economic importance in the area today, feed on phytoplankton and zooplankton.

1. Institute of Marine Research, S-453OOLysekil, Sweden. 2. Programa Cooperativo Pemano-Aleman de Investigaci6n Pesquera (PROCOPA), Instituto del Mar del Peru, Callao, Peru. 3. PROCOPA and University of San Marcos, Lima, Peru. 263 264 lournal of Marine Research [41, 2

PERU

,,. PACIFIC

Figure I. The study area. Benthic stations considered in this paper are marked with filled circles. Oxygen measurements were made at these stations and also at those marked with open circles. Depth contours in fathoms.

The decline in biomass of these pelagic planktivorous fish may have resulted in an increased input of decaying primary production to the benthic system. Walsh (1981) presented evidence for an increase over a 100year period in sulphate reduction at the sea bed, a decline in oxygen and nitrate content of the water column, and showed, as did Rowe (1981), an increase in sediment organic matter over this same period. The oxygen concentration in the upwelling area varies somewhat seasonally and between coastal areas. The oxygen conditions in the pelagic zone have been de- scribed by Gallardo (1963), Bogdanov (1972) and Zuta et al. (1978). From the surface down to approximately SO m the oxygen concentration decreases gradually 1983] Rosenberg et al.: Benthos biomass 265 from about 5 to 2mll-t, and in some cases to 0.5 mII-1• Below 100 m, oxygen may be less than 0.5 mll-1 down to approximately 600 m. At greater depths the oxygen concentration gradually increases. No clear seasonal variation in the oxygen concentration has been observed (Zuta et al., 1978). Oxygen values close to the bottom are lower than in the open sea according to Bogdanov (1972), and his results have been confirmed in this study. Oxygen values below 1 mll-1 have a clear impact on the benthic fauna. These values are encountered at about 20 m. The salinity in the area is around 35%0 with an annual maximum range of 2%0 from the surface to below 1000 m. The temperature in the nearshore zone varies between 16 and 23°C. It is lower (14-17°C at the surface) in the centers of upwelling plumes a little offshore, and between 13 and 18°C at a depth of 100 m. The 1Q°C-isotherm is located at a depth of 350-450 m and the 5°C-isotherm at 800- 1000 m (Sears, 1954; Zuta et al., 1978). An increased input of organic material to the benthic system over the past 10 years could theoretically have two effects. It might result in higher production of benthic animals and demersal fish at depths above and below the zone of extreme oxygen deficiency. On the other hand, increased organic loading at the· bottom might extend the zone of oxygen deficiency. In the latter case the zone of the sulfide biome would increase in area. The bottom regions of oxygen deficiency are known to be inhabited by sulfur bacteria (procarlota), mainly of the genus Thioploca, which in some places cover the bottom surface and provide a large proportion of the total biomass (Gallardo, 1976, 1977, 1979). At present no predictions can be made about the impact an increased detrital food supply might have on the benthic system and its demersal fishery. Landings of demersal fish, mainly hake (Merluccius gayi peruanus), have increased during the last decade, commonly surpassing 100,000 metric tons. However, this increase might just as well reflect an increase in the fishing effort of the demersal trawler fleet. The aim of this paper is to briefly summarize previous results on benthos from the Peruvian-Chilean upwelling areas and, in addition, present recent biomass data on coastal water macrobenthos down to 360 m depth.

2. Previous macrobenthic studies Quantitative benthic faunal analysis reported for areas off Peru and Chile give, in general, abundance and biomass data but complete lists of species or species numbers are not given. Methods used in the various investigations vary, but for purposes of rough comparison these differences are ignored. All biomass weights given in this paper are in wet weight. Near the Peruvian coast one transect was sampled between 126 and 6229 m at 6-9S (Frankenberg and Menzies, 1968) and another between 73 and 5700 m at 266 Journal of Marine Research [41, 2 about ISS (Rowe, 1971a, 1971b). The objectives of these two investigations were mainly to determine whether benthic biomass was inversely related to depth, as was observed in other upwelling and nonupwelling regions. Such a depth-biomass rela- tionship was found applicable also to Peruvian waters, but samples taken in the extreme oxygen-deficient zone deviated from the general depth trend. Frankenberg and Menzies (1968) recorded the highest abundance and biomass at the shallowest (126 m) station: 2308 indo m-2 and 40.3 g m-2, respectively. A small cirratulid polychaete dominated numerically (96 %). This station was men- tioned to be near the upper limit of what they called the "oxygen minimum zone." At 519 and 995 m depths, biomass dropped to 2 and 4.5 g m-2, respectively. Rowe (1971b) similarly recorded 57 g m-2 at 85 m, which was followed by 0.6 g m-2 at

300 m, where the oxygen concentration was below 1 mIl-1• At 875-1000 m bio- 2 mass was 165-205 g m- • Nematodes accounted for 97% of the abundance at depths between 126 and 995 m. Romanova (1972) sampled 115 stations along the Peruvian coast in 1972. The results of this extensive study were presented as biomass zones of 0 g, < 10 g, 10- 2 50 g and > 50 g m- • In the central parts (10-15S) a zone without macrobenthos and oxygen concentrations of < 0.2 mll-1 was found between 140 and 390 m. 1"'lorthand south of this zone small "worms" were the dominants, in general with 2 a biomass of < 10 g m- • At depths greater than 400-500 m the biomass was in 2 most cases> 50 g m- , and faunal dominants were large polychaetes, actinians, ascidians and sponges. ; In Chilean waters quantitative benthic samples have been taken between 50 and 282 m at 19-21S (Gallardo, 1963), and between 3 and 200 m at 23S in the southern limit of the upwelling area (Ramorino and Muniz, 1970). Gallardo (1963) obtained his samples in a low oxygen zone, generally < 0.3 mIl-i. As a result, the mean numbers and biomass for the area were low, 6.6 indo m-2 and 0.17 g m-2, respectively. Ramorino and Muiiiz (1970) report a high biomass of 450 g m-2 at 3-20 m depth in a 1.7 mll-i oxygen zone. Molluscs dominated the area. At greater depths biomass gradually decreased with decreasing oxygen. Between 121-200 m the oxygen concentration was 0.5 mIl-i and no macrofauna were found. The abundances in all these investigations do not show any clear relation to depth nor to oxygen. One reason for this is that some small components of the fauna, i.e., cirratulids and nematodes, were abundant in some hauls. The numbers of individuals are difficult to compare, because the mesh sizes of the sieves used in the different investigations affect the number of small specimens retained. Biomass values are less affected by different methods of sampling. These data are plotted against the oxygen concentration in Figure 2, including depths from 3 to 1000 m. A positive significant (p < 0.001) correlation is obtained between biomass and oxygen content. There is no significant correlation with depth, and the three maximum biomass values correspond to depths of 20, 875 and 1000 m. A 1983] Rosenberg et al.: Benthos biomass 267

BIOMASS 9 m-2 1000

500 o

100 o 50

10 5

1 0.5

0.1 o o 1 2 OXYGEN CONC. mll-1 Figure 2. Macrofaunal biomass in relation to oxygen concentrations in previous investigations. Data from Gallardo (1963) D. Rowe (1971b) A, and Ramorino and Muiiiz (1970) O. Oxy- gen values for Rowe were obtained from his Figure 1 (1971a). The curve was fitted by eye.

critical oxygen concentration for the benthos in this area seems to be around 0.6 1 mIl- • However, it must be taken into account that oxygen normally is not measured just at the bottom, but rather some distance above. Also, it is not reported in these papers whether the filamentous sulfur bacteria were included in the biomass measurements or not. Gallardo (1976, 1977) recorded a maximum biomass of this bacteria of about 1000 g m-2 at 60 m off the Chilean coast and reported their presence at various places from 14S to 36S at depths between 32 and 282 m. 268 /ournal of Marine Research [41. 2

Table 1. Basic data from cruise R.Y. Humboldt 8103-04, in March and April 1981.

Biomass Biomass Catch Totalorg. filamentous macro- demersal Station Depth 0. content bacteria benthos fish no. m mll-' % g 0.1 m-l g 0.1 m-l kg/20 min.

1 72 0.83 5.9 0.00 2.95 647 2 45 1.35 4.6 0.00 6.55 154 3 91 n.s. 2.8 0.00 24.72 (0)· 4 230 no sample 175 5 75 1.20 5.7 0.00 6.07 1174 6 62 1.56 4.8 0.00 3.48 47 7 90 1.57 3.2 0.00 1.75 158 8 86 1.38 4.8 no sample 95 9 344 0.68 6.4 0.00 1.16 158 10 359 n.s. 15.1 0.00 0.24 109 11 64 0.87 7.5 0.00 3.01 26 12 196 0.80 no sample 423 13 255 0.62 5.9 no sample 7 14 42 1.14 7.2 0.00 4.28 50 15 145 1.00 6.7 0.00 1.66 1762 16 187 0.78 n.s. 0.00 2.43 196 17 95 1.46 2.7 no sample 85 18 51 1.10 2.3 no sample 0 19 105 0.84 no sample 4357 20 81 1.22 2.6 no sample 1927 21 48 0.52 2.6 0.00 4.17 15 22 60 0.66 6.2 0.00 7.18 64 23A 40 0.47 2.1 0.00 5.94 no catch 23B 40 0.47 2.1 0.01 7.95 185 24 47 0.78 7.1 0.00 11.28 385 25 35 0.68 2.7 0.00 2Q.42 163 26 113 0.37 4.2 0.00 4.98 840 27 52 0.55 3.6 0.04 9.67 45 28 46 0.45 4.1 0.04 (15.47)" 7000 29 62 0.43 3.5 0.08 3.25 20 30 78 0.62 5.2 0.06 7.87 17 31 87 0.51 3.3 0.00 5.01 4987 32 128 0.55 4.5 0.01 2.28 207 33 138 0.38 5.0 0.00 1.95 11 34 163 0.38 5.0 0.04 2.78 2 35 283 0.51 6.6 0.Q3 0.22 0 36 72 0.48 3.5 0.Q3 2.78 4 37 66 0.37 4.2 0.00 2.04 24 38 81 0.36 5.4 0.10 2.31 7 39 100 0.43 7.2 0.01 4.06 4 40 136 0.56 7.0 0.00 3.35 24 41 160 0.58 8.7 0.00 9.60 327 1983] Rosenberg et al.: Benthos biomass 269

Table 1. (continued)

Biomass Biomass Catcb Totalorg. filamentous macro- demersal Station Depth O. content bacteria benthos fish no. m mll-1 % gO.1 m.•.•• gO.1 m.•.•• kg/20min.

42 251 0.36 9.6 2.98 1.26 18 43 123 0.59 6.8 0.15 1.87 7 44 88 0.52 4.3 0.00 4.71 14 45 50 0.28 2.3 10.76 0.39 23 46 56 0.41 2.8 0.04 1.79 10 47 63 0.42 3.1 10.26 2.46 14 48 65 0.37 3.1 5.28 2.83 0 49 67 0.34 7.7 1.30 1.53 0 50 96 0.86 4.9 0.15 0.95 0 51 109 0.63 6.4 0.84 2.89 11 52 111 0.21 n.s. 0.08 4.34 60 53 119 0.32 10.6 0.05 3.44 52 54 82 0.36 4.3 8.24 14.87 18 55 113 0.35 8.1 0.17 0.43 12 56 133 0.42 no sample 2 57 253 0.35 10.8 0.39 1.37 0 58 174 0.38 n.s. 0.82 3.23 129 59 182 no sample nocatcb 60 153 0.47 9.3 0.71 2.61 84 61 250 OS5 7.4 0.02 1.87 25 62 166 0.51 6.3 0.00 4.75 115 63 87 0.47 4.7 6.64 2.41 0 64 93 0.42 4.6 2.89 0.82 0 65 104 0.27 3.2 3.69 0.14 0 Note: Station numbers are from N to S (see Fig. 1). A map with station numbers can be obtained from Instituto del Mar del Peru. "No sample" (n.s.) means that benthic sample was not quantitative; viz., O. sample W:asnot taken. • Net broken . •• 10.26 g was limpets on a stone.

3. Material and methods The material for the present study is mainly derived from four cruises with R.V. Humboldt in October and December 1980, and March-April and May-June 1981 (Fig. 1). Additional material from shallow water was sampled in the Bay of Ancon, north of Lima, between January and September 1981. In addition, data on organic carbon are included from a recent study by Rowe (1979). From the Humboldt cruises 8010, 8012 and 8105-06, to date only oxygen values (Winkler method) determined by the Oceanographical Department of Instituto del Mar del Peru (IMARPE) are available. Cruise 8103-04 included measurements of oxygen, organic content of sediment, biomass of sulfur bacteria, biomass of macrobenthos and 270 Journal of Marine Research [41, 2 fish catches. The stations during this cruise were chosen at random from the northern .border to north of Callao comprising a total of 141 stations, 65 of which (Pto. Pizarro-south of Chimbote) are presented here (Fig. 1; Table 1). Macrobenthic biomass and sulfur bacteria samples were taken with a 0.1 m2 van Veen grab fitted with additional weights. During the 8103-04 random station sur- vey, one benthic grab sample was taken at each station at depths between 35 and 360 m. The filamentous structure of the sulfur bacteria permits their retention on a sieve. Grab samples were sieved through a 1 rom2 mesh after collecting a sub- sample for analysis of organic content. Biomasses of fauna and bacteria were measured after blotting on filter paper; wet weight included mollusc shells but not tubes of polychaetes. Total organic content of the sediments was analyzed after drying at 105°C and combustion at 500°C for one hour (Dean, 1974). Water samples for oxygen determination were taken by 5 I Niskin bottles within 1 m from the bottom simultaneously at each station. Fish catches were made over a 20 minute trawling period using a demersal trawl (opening ca. 6 m, distance between the wings ca. 20 m) with a narrow mesh in the codend. Shallow water samples in the Bay of Anc6n were taken by divers using a 200 cm2 corer, and by a 0.04 m2 van Veen grab lowered by hand from a boat. Treatment of the samples was similar to those obtained on R.V. Humboldt but the samples were washed through a 0.5 rom sieve. For correlating the different parameters, Spearman's rank correlation test (Sachs, 1978) was used as the data cannot be ex- pected to be randomIy distributed. For the same reason, the difference between means was examined using a Mann-Whitney V-Test (Elliott, 1979).

4. Results Oxygen. Oxygen was measured on three expeditions with R.V. Humboldt in Oc- tober-December 1980, March-April 1981 and May-June 1981 at depths between 20 and 1020 m (Fig. 3). In the northern part of the upwelling zone, between 3°30' and 6°20'8, oxygen concentrations were above 0.6 mII-i and in general higher than south of this area. In the main part of the surveyed area, between 6°30'S and 15°30'S, oxygen concentrations were between 0.1 and 1.0 mll-i at depths down to about 1000 m. Most of the values were between 0.3 and 0.6 mIl-i. At about 1000 m concentrations of 1.2 to 1.7 mll-i were recorded. No clear seasonal differences were noted between surveys. However, the variation in the data between 20 and 100 m could be a matter of seasonality. Oxygen values in shallow waters in the winter (20 m up to the shoreline) were high; 2 to above 5 mll-l, They decreased dramatically, however, between 15 and 20 m in summer, with most values falling below 0.5 mIl-i. Organic material in sediments. Organic carbon was analyzed in the 0-3 cm sedi- 1983] Rosenberg et al.: Benthos biomass 271

OXYGEN CONCENTRATION ml r1 .1 13.9

2. •

a 1.6 •a • • o 1.2 • • • • • o •• • o 0 • 0 0 Il. 0· l .• ~ • Il. o Il.

Il. = Il. 8 o Il. o 0 o 700 800 gx) 1000 1100

1 Figure 3. Oxygen concentrations (ml 1- ) close to the bottom off Peru in relation to depth. Humboldt cruises Oct. 1980: • 3°-6°30' S, <> 6°31'-12"00' S; Dec. 1980: • 3°-6°30' S, o 6°31'-12"00' S; March-April 1981: .•. 3°-6°30' S, .t!. 6°31'-12"00' S; May-June 1981: o 12"00'-15°30' S. Bay of Anc6n shallow water: '" Sept. 1981-June 1982. - Points are mean values except for data below 300 m which represent single measurements. Mean values represent 20 m classes in the case of Humboldt and 5 m classes for the AnOOn data.

ment layer in the depth range 32-4110 m between latitudes 5°30' and 15°30'S (Rowe, 1979). At depths less than about 100 m organic carbon was less than 3.5% (Fig. 4). At greater depths the values were higher, generally between 3.5 and 10%. This trend was found to be highly significant (p < 0.001). Data on the sediment organic content in this study, which were sampled simu1- taneously with the benthic fauna, apply to a depth range between 35 and 360 m. The organic content varies, with one exception, between 2 and 11% and shows also a significant increase with depth (p < 0.001). 272 lournal of Marine Research [41, ·2

ORGAN IC CONTENT 0 15 15 ORGANIC CARBON • l' l' 0 0 • % 0 10 • 0• 0 0 8 Cb 0 • 0 o 00 00 • o· • • 0 (00 '<9 • 6 0 ttl 0 • 00. , • • • 00q{5 ~o • •• 00 • 4 00 ." • 000 oo~ • • o 00. ~.o B 2 , •• • O+-,.....--~-,-----,---r---..,..• • o 10 SO 100 500 1000 5000 DEPTH m Figure 4. Percentage organic carbon (.: 6-158) and organic content (0: 3°-9°30' S) in relation to depth. Organic carbon was measured in the top 3 cm of the sediments in 1976 and 1978 and is adopted from Rowe (1979). Organic content was analyzed in March-April 1981 at the benthic stations indicated in Figure 1.

Organic content (loss on combustion) is related to organic carbon content by a factor of at least two. As the two sets of samples were not taken in the same area, it is not possible to show any increase or decrease over the five year period presented in Figure 4. Benthic biomass. Biomass of benthic macrofauna and filamentous sulfur bacteria, predominantly Thioploca according to Gallardo (1977), are presented in Table 1. In the investigated area north of 6°30' (stations 1-25), with its comparatively higher oxygen concentrations (Fig. 3), no Procariota were found. South of this latitude filamentous bacteria were present in most of the samples at depths between 46 and 283 m. Highest biomass values of this bacteria were recorded at 50-104 m depths between 7° and 9°30'S. However, the distribution of Thioploca is known from other Humboldt expeditions to extend southward at least to San Juan (16S). Macrobenthic biomass averaged 4.5 g 0.1 m-2 for the area between 3°30' and 9°30'. Arranging stations according to their depths shows that stations above 100 m 2 had a comparatively higher biomass (mean 5.9 g 0.1 m- ) than those between 100 2 and 200 m (mean 3.1 g 0.1 m- ). The mean for the 6 stations below 200 m was 2 even lower (1.0 g 0.1 m- ). A division between stations north of 6°30' and those 1983] Rosenberg et al.: Benthos biomass 273

MACRO BENTHIC BIOMASS 9 0.1m-2 20 •

15 •

• 10 .0 • • • • • 5 0 \l, 0 0 • • 0 0 0 • • 0 0 •• ~ 0 ~:- 00 0 ~ • 0 0 0 0 o • 0 o o 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 OXYGEN CONCENTRATION mll-1

Figure 5. Macrobenthic biomass as g wet weight per 0.1 m' in relation to oxygen concentration (mll-'). Samples obtained between 35 and 85 m depth indicated by filled circles and samples from 86-359 m by open circles.

south of this latitude (Stas. 26-65) reveals a higher biomass (6.4 g 0.1 m-2) at 2 northern stations relative to southerly ones (3.4 g 0.1 m- ; p < 0.05). Polychaetes were the most important macrobenthic group contributing 72 % of the biomass followed by molluscs with 12 and crustaceans with 7 %. These values change little with latitude, although in the north crustaceans were somewhat higher in biomass, whereas molluscs gained in importance in stations south of 6°30'. The remaining 9% by weight, was mainly contributed by nemerteans. Due to the mesh size of 1 mm, a proportion of the small polychaetes and the nematodes may not have been quantitatively sampled. The macrobenthic biomass data are plotted against oxygen concentrations in Figure 5. Biomass was, with one exception, lower than 5 g 0.1 m-2 at oxygen concentrations of less than 0.45 ml 1-1. In high oxygen conditions biomass was in 274 lournal of Marine Research [41, 2 general higher, and the highest values were frequently found at depths between 35 and 85 m. The mean biomass in this depth zone was 7.4 g 0.1 m-2 and significantly (p < 0.05) higher than the mean of 2.9 g 0.1 m-2 found between 86 and 360 m. The highest biomass values were found in the northern half of the surveyed area. No sites were found to lack ~ 1.0 mm macrofauna among the 65 stations worked-up to date. Fish catches are negatively correlated to the occurrence of filamentous bacteria (p < 0.01) and positively correlated to high macrobenthic biomass (p < 0.001). At stations with Procariota some macrobenthos are always present, but the biomass values are negatively correlated (p < 0.01). In the Bay of Ancon, benthic samples were taken in February, July and Septem- ber 1981 at depths between 8 and 32 m. In the shallower half of the area, biomass 2 varied between 0.5 and 64 g 0.1 m- • Most of the samples had values greater than 2 5 g 0.1 m- , and in cases when molluscs were caught (mainly Ameghinomya) biomass increased 5-10 times. When the corer was used for benthic sampling the biomass of these molluscs was not always quantitatively assessed because of the small size of the corer. Divers observed rather dense populations of molluscs all over the area and the biomass may be generally high. At 21 m the bottom was covered with a white "lawn" of filamentous bacteria, mainly Thioploca but perhaps also one more genera, with a bacterial biomass of 2.6 g 0.1 m-2, and with few other animals. 2 At 32 m biomass was less than 0.2 g 0.1 m- • Oxygen was measured to be below 0.5 mll-1 in the depth range of 15-34 m. s. Discussion and conclusions The highly productive upwelling system off Peru and Chile is fueled by high primary production, which may exceed 1000 g m-2 yr-1 (Walsh, 1981). A fraction of this production not incorporated into fish biomass will sink to the bottom. This detrital input appears to be high as reflected by generally high organic contents in the sediments (Fig. 4), and an increase in the rate of organic loading may have occurred after the population decline of the anchovy population (Walsh, 1981; Rowe, 1981). In a recent investigation (Rowe, 1979) and in this study, the organic content of bottom sediments between 30 and 100 m were lower than below about 100m (Fig. 4). Thus, organic material may accumulate more rapidly in water depths ~ 100 m off Peru. Oxygen concentration near the bottom between 20 and 700 m is generally less than 0.8 mll-1 and in most cases less than 0.6 mll-1 (Fig. 3). The surplus of detritus which the benthic system receives cannot be fully utilized by the macrobenthos due to the low oxygen. Therefore, the biomass of macrobenthos is low in the whole zone of low oxygen values and, in spite of very good food conditions for the benthos, high biomass values appear only near shore (0-2 m) (penchaszadeh, 1983] Rosenberg et al.: Benthos biomass 275

1971). Up to 43 kilograms m-Z were provided by the bivalves Mesodesma, Donax and the crustacean Emerita. Possibly there are also comparatively higher biomass values in the part of the deep sea bordering upwelling areas as compared to deep-sea areas not influenced by upwelling (Thiel, 1978). The lowest biomass in the present study was recorded in oxygen concentrations of less than 0.45 mll-l. In previous investigations, reviewed in this paper, oxygen concentrations of less than 0.6 mll-1 seemed to depress biomass. A comparatively higher biomass was found in waters of less than about 80 m, and in the northern latitudes of the investigated area. However, the reason for this is most likely that the oxygen concentrations were permanently and/or periodically higher than at depths below about 80 m (and down to approximately 700 m), and probably also permanently higher in the northern areas off Peru. From this we can conclude that oxygen seems to be the dominant ecological factor in determining the biomass and species composition of the benthic system. Similar to the results reported above, Khusid (1974) found the highest organic content in sediments and the lowest oxygen concentrations « 0.5 mll-l) in a zone between a depth of 50 and about 700 m. Analysis of oxygen concentrations were made at IMARPE in 1964, 1969, and 1970 along the Peruvian coast. Our 1980- 1981 observations do not indicate that oxygen conditions close to the bottom have worsened recently; rather the values are similar to those recorded in 1964, 1969, and 1970. The role of oxygen in determining the distribution of benthic fauna in this upwelling area was first pointed out by Gallardo (1963). More recently, Frankenberg and Menzies (1968), Rowe (1971a, 1971b) and Thiel (1978) also mention the possible faunal impact of oxygen depletion, but these authors do not relate their quantitative faunal data to pOz but rather to depth. It is important that future benthic sampling programs in upwelling areas be accompanied by measurements of dissolved oxygen. Otherwise, interpretation about which ecological factors determine faunal distribution may be incomplete. Off the coast of Peru and Chile, benthic abundance and biomass were rather high in oxygen concentrations of between 0.6 and 2.0 mll-l (Figs. 2 and 5). Rhoads and Morse (1971) concluded from published results about other areas that azoic regions appear below values of 0.1 mll-1 and that a small, soft-bodied infauna of low diversity is found in oxygen concentrations of between 0.3 and 1.0 mll-t. In fiords in northwest Europe, abundance and biomass have been found to decrease drastically when the oxygen concentration drops below about 1.4 mll-\ and no macrofaunal species increase in numbers under these low oxygen conditions (Rosen- berg, 1980). Off the South American coast cirratuIids and nematodes are numerous in low oxygen areas (Frankenberg and Menzies, 1968; Rowe, 1971b), and in this study we found that a number of 'species are recurrently sampled in low oxygen areas (cf. Table 2). Thus, it seems that some species or genera have adapted to low 276 lournal of Marine Research [41, 2

';l o o on o -= t"- ...., ...., , .s ~ .... on .;.- .•.. - coo - I': en - o o '" N U

o o co N co ~ I o ..t .;.'" N U o* o N -

~ o U

on '"N '". 1\ .;. o -

N N -..t -v

oxygen conditions in the upwelling area. One reason for a successful adaptation to these conditions could be that oxygen deficiency probably has prevailed over long periods of time and through evolutionary adaptation, a low oxygen fauna has evolved. 1983] Rosenberg et al.o' Benthos biomass 277

=e ~ '"

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.... • 0 ~ .<::: o•• • «l.§ .~ = tIl·~ '" '" •..'" oj •• ::l ~- ~ 4) 4) 8 .~o .~> .5 ~ g~ oe 8,'1:1 § ~:I>O I •• i:Q CI.l Q

In the upwelling area off Peru and Chile five depth zones with different faunal component can be identified (Table 2). Most beach zones are affected by high wave forces, and the fauna living there exhibit special features (e.g., tidal migration, rapid burrowing) not only to survive in this environment, but this zone produces an ex- 278 Journal of Marine Research [41, 2 tremely high biomass. Sheltered beaches are inhabited by a different fauna, e.g., deep burrowed shrimps (Callianassa) and fragile polychaetes. Below the zone of direct wave action dissolved oxygen abruptly decreases at about 20 m (in some areas at 30-35 m). Turbulence may be the main physiologic stress factor in the upper part of this 0-20 m zone, and declining oxygen tension in the lower part. Faunal composition below 20 m is mainly influenced by oxygen deficiency. The bathymetric extension of this zone varies from area to area but seems to be most frequently encountered in the depth range of about 20-80 m. The fauna here are characterized by species tolerant of low oxygen. Periodically these species might be mixed with mobile immigrants and opportunists if p02 conditions improve. Below this zone and down to about 700 m more or less permanently low oxygen concentrations exist « 1 mll-1 and, in some cases < 0.6 mll-1 (Fig. 3». The filamentous sulfur bacteria Thioploca is a conspicuous member of the sulfur biome found at many places in this zone, but in areas sheltered by islands Pro- cariota are found in shallower waters up to 10m. Beyond this zone (> 700 m) oxygen concentrations gradually increase and the deep-sea zone begins. The deep- sea benthos in this region have not been investigated recently, but the results of previous investigations give some indications that the deep-sea benthic biomass off Peru might be higher than in other nonupwelling areas (Thiel, 1978).

Acknowledgments. This is PROCOPA publication no. 2.

REFERENCES Bogdanov, D. V. 1972. Investigaciones cientffico-pesqueras en las aguas del oceano pacifico adyacentes a la costa del Peru durante el inviemo de 1972. Condiciones hidrol6gicas. Ser. Inf. Esp. IMARPE 128 (mimeo), 24-99. Dean, W. E. 1974. Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: Comparison with other methods. J. Sed. Petrol., 44, 242-248. Elliott, J. M. 1979. Some methods for the statistical analysis of samples of benthic invertebrates. Freshwater Biological Association, Scientific Publication No. 25, 144 pp. Frankenberg, D. and R. J. Menzies. 1968. Some quantitative analysis of deep sea benthos off Peru. Deep-Sea Res., 15, 623-626. Gallardo, A. 1963. Notas sobre la densidad de la fauna bent6nica en el sublitoral del norte de Chile. Gayana (Zoo!.) 10, 3-15. -- 1976. On a benthic sulfide system on the continental shelf of north and central Chile, in Proc. Intern. Symp. Upwell. Coquimbo, Chile 1975, J. C. Valle, ed., 113-118. -- 1977. Large benthic microbial communities in sulphide biota under Peru-Chile subsurface countercurrent. Nature, Lond., 268,331-332. -- 1979. EI bacteriobentos de la plataforma continental de la costa sur-occidental de Sud- america: un reciente descubrimiento, in Memorias del Seminario sobre Ecologia Bent6nica y Sedimentaci6n de la Plataforma Continental del Atlantico Sur. UNESCO. Montevideo, 259- 267. Khusid, T. A. 1974. Distribution of benthic foraminifers off the west coast of South America. Oceano!., 14, 900-904. 1983] Rosenberg et al.: Benthos biomass 279

Pencbaszadeh, R. 1971. Observaciones cuantitativas preliminares en playas arenosas de la costa central del Peru, con especial referencia a las poblaciones de muy-muy (Emerila analoga) (Crustacea, Anomura, Hippidae). Inst. BioI. Mar, Mar del Plata. Contrib. 177. Ramorino, L. and L. Muniz. 1970. Estudio cuantitativo general sabre la fauna de fondo de la Bahia de Mejillones. Rev. BioI. Mar. Valparaiso, 14, 79-93. Rhoads, D. C. and J. W. Morse. 1971. Evolutionary and ecological significance of oxygen- deficient marine basins. Lethia, 4, 413-428. Romanova, N. N. 1972. Investigaciones cientifico-pesqueras en las aguas del oceano pacifico adyacentes a la costa del Peru durante el inviemo de 1972. Distribuci6n de bentos en la plataforma y en el talud continental de la costa peru ana. Ser. Inf. Esp. lMARPE 128 (mimeo), 127-132. Rosenberg, R. 1980. Effects of oxygen deficiency on benthic macrofauna, in Fjord Oceanog- raphy, H. J. Freeland, D. M. Farmer and C. D. Levings, eds., Plenum, N.Y., 499-514. Rowe, G. T. 1971a. Benthic biomass in the Pisco, Peru upwelling. Inv. Pesq., 35, 127-135. -- 1971b. Benthic biomass and surface productivity, in Fertility of the Sea, Vol. 2, J. D. Costlow, ed., Gordon and Breach Sci. Publ. N.Y .• 441-454. -- 1979. Sediment data from short corers during Joint II off Peru. Coastal upwelling eco- system analysis, data report 65, 53 pp. -- 1981. The benthic processes of coastal upwelling ecosystems, in Coastal Upwelling, F. A. Richards, ed., American Geophysical Union, Washington, D.C., 464-471. Sachs, L. 1978. Angewandte Statistik. Springer-Verlag, Berlin. Sears, M. 1954. Notes on the Peruvian coastal current. 1. An introduction to the ecology of Pisco Bay. Deep-Sea Res., 1, 141-169. Thiel, H. 1978. Benthos in upwelling regions, in Upwelling ecosystems, R. Boje and M. Tom- czak, eds., Springer-Verlag, Berlin, 124-138. Walsh, J. J. 1981. A carbon budget for overfishing off Peru. Nature. Lond., 290,300-304. Zuta, S., T. Rivera and A. Bustamante. 1978. Hydrologic aspects of the main upwelling areas off Peru, in Upwelling ecosystems, R. Boje and M. Tomczak, eds., Springer-Verlag, Berlin, 233-257.

Received: 19 lt1nutIT)', 1982; revised: 61anutlT)', 198J.