A Trophic Model for Tongoy Bay - a System Exposed to Suspended Scallop Culture (Northern Chile)

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY Journal of Experimental Marine Biology and Ecology AND ECOLOGY ELSEVIER 182 (1994) 149-168

A trophic model for Tongoy Bay - a system exposed to suspended scallop culture (Northern Chile)

Matthias Wolff

Zentrum fir Marine Tropeniikologie. Klagenfurter Str. GEO, 28359 Bremen, Germany

Received 1 November 1993; revision received 14 March 1994; accepted 25 March 1994

Abstract

A steady-state model of 17 compartments was constructed for the Tongoy Bay ecosystem using the ECOPATH II software of Christensen & Pauly (1992). The system is driven by planktonic production which is governed by periodical intrusions of upwelling water from a nearby upwelling centre. Of the total system biomass (236.3 g/m’), 47% is comprised of benthic invertebrates whose food intake exceeds that of pelagic fish and birds. Scallops in hanging cultures account for 7104 of the biomass in the water column. The model suggests that benthic invertbrate predators are more important in the cycling of biomass than demersal fish. A significant part of the production of the groups Macrophytes, Zooplankton, Phytoplankton, Suspended Scallops and a minor portion of other groups enters the detritus pool, from which an important amount of biomass re-enters the filter feeder compartments through bacteria. Global system properties such as total system through put(T), development capacity (C), ascendency (A) (sensu Ulanowicz & Mann, 1981; Ulanowicz, 1986; Baird & Ulanowicz, 1993) were also calculated by the means of net work analysis implemented in the ECOPATH II software. Results indicate that Tongoy Bay is an intermediate sized system (in terms of the sum of flows, T) of low maturity and high capacity to withstand ecological perturbations. The mean transfer efficiency between trophic levels is 14.7x, the fishery’s gross efficiency (primary production/catch and harvest) is 0.897”. In terms of global system properties these results are similar to those reported by Jarre et al. (1991) for the “open” Peruvian upwelling system during the peak period of anchovy catches (1963-1969). However, the mean trophic level of the fishery (3.6 for Tongoy Bay compared to 2.2 for the open upwelling system) and the biomass pathways differ significantly between these systems. Manipulation of the input data suggest that the bay has a potential for the production of biomass of filter feeders that is 10 to 15 times higher than the present production.

Keywords: Biomass budget; Ecosystem structure; Scallop culture; Upwelling

Tongoy Bay is a semi-enclosed shallow water embasement of about 60 km’ surface area located in Northern Chile (30” 14’30’s; 71 O30’ W). 40 km south of Coquimbo (Fig. 1). It is an important centre for tourism, fishing and invertebrate collection. Along its long beach (13.5 km) surf clams (Mesodesma donaciumn) are harvested intertidally by local fishermen and -women; subtidally an invertebrate diving fishery is operating. Its main target is the scallop (Argopectenpuvpurutus), whose largest banks of Chile are located here, but crabs (Cancerpol’odon) and snails (Xunthochonts sp.) are also col- lected. About 50”; of the pelagic and demersal fish landed in the fishing port of Tongoy is caught within the bay. Over the past years, scallop hanging cultures have increasingly become important. At present, several million scallops are suspended in the water column. Although some seed is artificially produced in hatcheries in Chile, most seed still comes from spat collectors or from the natural banks of the bay, were juveniles are clandestinely col- lected. The input of “unnatural” amounts of biomass through the scallop cultures into the system is most likely to significantly alter the biomass structure and trophic flows of the ecosystem and the question about the sustainability of the cultures and fisheries must be asked. While research has been done on the oceanographical conditions of the bay (Olivares et al., 1979; Olivares & Moraga, 1988; Acufia et al., 1989), and on most of its biotic compartments: plankton (AcuiIa et al., 1989; Alcayaga, 1990; Richter, 1990); scallop populations and other subtidal epibenthic macrofauna (WoIff & Alarcon, 1994); intertidal surfclam (Mesodesma donacium) populations (Alarcon, 1979) etc. no attempt has as yet been made to integrate the available information into a quantitative ecosystem model and to understand the main energy pathways of the system. Such an attempt is presented here, which was motivated by the following questions: (1) How is the biomass and biomass flow structure of this scallop dominated bay? (2) What are the main benthic predators, their prey items and consumption rates? (3) What is the amount of suspended scallop biomass compared to other filter feeders of the system? (4) What is the carrying capacity of the bay in terms of available food for filter feeders? (5) Which are the compartments most likely affected by the scallop cultures? (6) How do the energy fluxes within this bay differ from the open upwelling system? To model the bay’s ecosystem, the ECOPATH II software of Christensen & Pauly (1992) was used, which combines an approach of Polovina (1984) for estimation of biomass and food consumption of the various ecosystem elements (species or species groups) with an approach proposed by Ulanowicz (1986) for analysis of flows between the elements of an ecosystem and for the calculation of ecosystem indices. Among these are “Total System Throughput (T)“, which reflects the size of the system in terms of the sum of flows through all the individual compartments, “Ascendency (A)” which represents both the size and the organization of the flows and the “Development capacity (C)” which is the upper limit to ascendency. The degree of a system’s realized growth, organization and development can be given by the A/C ratio (Ulanowicz & Mann, 1981). Highly organized systems have the tendency to internalize most of their activ- ity and exchanges and become relatively independent of external inflows and outflows Fig. 1. Tongoy Bay. The upwelling centre ““Pta. Lengua de vaca” is located in front of Pta. Lengua de vaca. (Baird & Ulanowicz, 1993). The A/C ratio appears to be high in well organized systems possessing significant internal stability which makes it difficult for new influences to change its basic structure, and lower in systems under stress. These indices have thus been used to compare ecosystems of different sizes, geographical location and com- plexity (Baird et al., 1991; Ulanowicz & Wulff, 1991). In the ECOPATH II model, biomass production of and imports to thecompartments is balanced by consumption and exports. Important input parameters for the model are: biomass (B), production per unit of biomass (PB), consumption per unit of biomass (QB), ecotrophic efficiency (EE) - the fraction of the production used in the system - and export (EX). Respiration (R), respiration per unit of biomass (R/B) and gross efficiency (GE) are output parameters that are crucial for examining the modelling results. The modeller defines the modet structure by a prey-predator matrix indicating the fractions of the total consumption coming from each prey source.

2. Material and methods

2. I. The study area

The bay is influenced by a nearby upwelling centre (“lengua de vaca”, Fig. 1) which provides periodical intrusions of nutrient rich upwelling water (Acuda et al., 1989). Strong daily winds in the afternoon maintain a high water circulation. Water temperatures range from about 9 ‘C in the bottom waters in winter to 19 “C in the surface waters in summer (annual average: 14.6 “C). Under summer conditions of high radia- tion and weak winds, a thermocline develops up at about 10-l 5 m water depth, separating warm surface water ( 16- 19 ‘C) from colder bottom water (12- 15 ‘C). Oxy- gen concentrations usually exceed 409; saturation even in bottom water above 25 m. The deepest part of the bay measures 90 m, the average depth is around 25 m. In the lower parts of the bay (> 30 m) anoxic conditions occasionally exist during the late summer months. About 70?,, of the bay’s sediment is made of fine sand (average grain size 288 p) with an organic content ranging from 0. l- 1.09, (Pacheco et al.. 1987) but gravel bottom and sand mixed with shell debris can also be found as well as areas with stones (Wolff & Alarcon, 1994). These harder bottom areas are partly covered with macrophytes. Wolff & Alarcon (unpubl.) estimated an average macrophyte biomass in the bay of 25 g . m ’ (wet weight). In the northern sandy part of the bay small eel- grass beds extend over an area of = 3 ha. Nitrate, nitrite and phosphate concentrations increase with depth. In the depth range of 20 to 25 m they were measured as 10.5,0.38 and 1.42 pg at/l, respectively (Pacheco et al., 1987).

2.2. Basic modeling approach

The core routine of ECOPATH II basically consists of using a set of simultaneous linear equations (one for each group i in the system), i.e.: Production by i-, all predation on i-, non-predation losses of i-. export of (i) = 0. for all i, M. Wolff/ .I. Exp. Mar. Biol. Ecol. 182 (1994) 149-168 153

or:

Pi - BiM2i - Pi(l - EE,) - EX, = 0, (1) where Pi = the production of (i); Bi = the biomass of(i); M2i = the predation mortality of (i); EEi = the Ecotrophic Efficiency of (i); l-EE, = the “other mortality”; EX, = the export of (i). Thus, the biomass production (Pi = Bi.PBi) is the amount available to the system. Most of it will be used by predation (Bi . M2,), but a certain amount might be lost through other mortality [Pi(l - EE,)] or as export to other systems (EX,), i.e. through sedimentation or the fishery. The compartment is connected to its food compartments by its consumption (QBi). Thus, Eq. (1) can be re-ex pressed as:

Bi.PBi.EEi - CjBj.QBj.DCji - EX; = 0 (2) where PBi is the production/biomass ratio, QB, is the consumption/biomass ratio of the predator j and DCji is the fraction of the prey (i) in the average diet of predator j. Two of the three parameters B, PB and EE have to be set initially for each group. The remaining parameter is computed by the software. Particularly for some lower- trophic level organisms, EE is sometimes changed by the program, even when P or PB are treated as initial unknowns. QB of a compartment can also be calculated and treated as an unknown in initial parametrization, if certain information is available for prey compartments. For further details of the ECOPATH II model structure see Christensen & Pauly (1992).

2.3. Selection of model groups (compartments)

As a first step in defining the model compartments, all available information on biomass, catches, P/B ratios, consumption rates (Q/B), as well as growth and mortality rates for the species/groups of the system was assembled from the literature, landing statistics and own research data. As a next step, species of similar sizes, diets, consumption rates, mortality and production rates were grouped within a compartment. As a result, a 17-compartment model was developed (Fig. 2) consisting of the following groups: (1) Birds, (2) Chilean Yellowtail, (3) Chilean Warehou, (4) Horse Mackerel, (5) Small Pelagics, (6) Large Demersals, (7) Small Demersals (8) Predatory Snails, (9) Predatory Crabs, (10) Bivalves (> 1 cm), (11) Suspended Scallops, (12) Large Echi- noderms (13) Small Benthos (< 1 cm), (14) Macrophytes, (15) Zooplankton (16) Phy- toplankton, (17) Bacteria. Table 1 contains these groups with their main elements and summarizes the parameter values obtained and used as initial input for the ECOPATH II program. Information to set the predation matrix was taken from literature sources, unpub- lished university reports and from personal observations (Groups 1, 7, 11). For the phytoplankton biomass, the following conversions were used: Chl-a to carbon, 25:l; carbon to dry organic matter, 1:2.5; dry to wet weight organic matter, 1:5 (Parsons et al., 1977). For the biomass/m’ estimates for phytoplankton, zooplankton and bacteria, the average water depth of the bay (25 m) was considered. _~___ ._._._ _ .“_..___-- ...-. _--.---. _I --t------___------t-- t f- -- rr, mt c? -t

l3hB? 3ZHdOBL M. Wolff/J. Exp. Mar. Biol. Ecol. 182 (1994) 149-168 155

2.4. Balancing the model

The first step in verifying if the the model output was realistic, was to check if the ecological efficiency (EE) was < 1.0 for all compartments, as values > 1.0 are incon- sistent (it is impossible that more biomass is used than produced by a compartment); if inconsistency was detected, the B or PB values were adjusted; as a second step, the GE (gross efficiency) and R/B values were checked for their consistency by comparing them with literature data as were the missing Q/B, P/B values calculated by the program. As the biomass input values of the benthic invertebrate predators and that of the phytoplankton and zooplankton were considered quite accurately determined (the estimates were based on year around studies), it was decided not to significantly alter these input values during the balancing exercise.

3. Results and discussion

3.1. Evaluation of the compartment parameters

Fig. 2 shows the compartment model for the “balanced” Tongoy bay ecosystem. The boxes are aligned along the y-axis as a function of the estimated trophic level and the area is proportional to the square root of the biomass. Table 2 summarizes the input values for the final run and those that were calculated by the program. The diet matrix used is shown in Table 3. Surprisingly few and small modifications had to be done with the input parameters to balance the model. A notable exception was the biomass value for the Small Benthos compartment that had to be increased 5-fold (from 8 to 40 g/m2). An explanation for the too low initial input value taken from Wolff & Alar-con (1994) is that the authors probably undersampled the small fauna as their sampling was oriented towards the larger scallops and their predators (> 10 mm size). The P/B values that were modified during the balancing exercise (for Warehou from 2.3 to 1, for Horse Mackerel from 1.2 to 1.35, for Predatory Snails from 1.1 to 1.925 and for Predatory Crabs from 2.1 to 1.8 seem realistic. The values of the invertebrate groups, however, are of an order of magnitude higher than when estimated by the empirical relations hip between P/B and size published by Schwinghamer et al. (1986). However, there is substantial evidence in the literature that P/B values around 2.0 or higher are possible for large macroinvertebrates of the Pacific coastal upwelling region. Wolff & Soto (1992) and Wolff (1989), for example, determined P/B of 2.1 for the Chilean crab Cancerpolyodon, and of 1.8 for the large gastropod Concholepas concholepas respectively. Arntz et al. (1987) reported a P/B value of 2.6 for for the surf clam Mesodesma donacium at a Peruvian beach. Urban (1992) reported P/B values around 2.6 for the bivalves Venus ant&a and Tagelus dombei. The discrepancy between these

Fig. 2. Trophic model of the Tongoy Bay ecosystem. The box size is proportional to the square root of the compartment biomass; numbers in parentheses represent the total amount of biomass entering the compartment; all flows are in gdrn -* (wet weight); for further explanation see text. : J. M. Wol@-/.I. Exp. Mar. Biol. Ecd 182 (1994) 149-168 157

* *

00 2 d d Table 1 (cwrtinued)

Species groups B c (P/B) Q/B GE Look k Source

( 13) Small benthos c 10 mm About 45 species 8* 4** 15** * Based on Wolff & Alarcon (1994), ** Estimate

( 14) Macrophytes Wolff & Aiarcon (unpubl.) Rhodymenia Gratelupia Wolff & Alarcon (unpubl.) Ulva Desmarestia Dendrimenia ** Macchiavello et al. (1987) group 25* j-10** * Wolff & Alarcon (unpubl.)

(15) Zooplankton Copepods Decapod larvae Balanid larvae Euphausids Apendicularia Chadognathes *** .4dapted from Polovina (1985) group IF aI** 160*** * Wolff & Aron (1991). ** Mendoza (1992)

( 16) Pkytoplankton Diatoms Dinoflagellates 1X0-255** f 17) Bacteria Water bacteria group 3.2* I oo-400** * After Watson ( 1978). ** After Valiela (198-l)

B = biomass: C = catch: P B = turnover rate; Q’B = annual food consumption: GE = gross efficiency; Look: von Bertalanffy growth parameters Table 2 Tongoy Bay

Catch Biom. P/B Q/B EE GE FI Net eff. R A R/A P/R R/B $q

(1) Birds 0.3 0.07 62 0 0.001 18.6 0.001 14.86 14,88 0.99 0.001 (2) Yellotait. 0.53 0.56 1 9.5 0.95 0.105 5.3 0.132 3.68 4.24 0.87 0.152 (3) Warehaw 0.87 0.92 1 6.8 0.95 0.147 6.23 0.184 4.07 4.98 0.814 0.225 (4) Horse Mackerel 14.3 14.46 1.35 14.2 0.95 0.095 205.3 0.119 144.7 164.2 0.881 0.135 (5) Small Pelagics 12.3 23.6 2.3 16.7 0.95 0.138 394.2 0.172 261 315,3 0.828 0.208 (6) Large Demersals 1.5 3 Oh6 3 0.833 0.2 9 0.25 5.4 7.2 0.75 0.333 (7) Small Demersals 1.2 3 1.5 4.9 0.952 0.306 14.7 0.383 7.26 11.76 0.617 0.62 2.42 & (8) Predatory Snails 0.7 4.2 1.925 5.5 0.913 0.35 23.1 0.438 10.4 18.48 0.563 0.778 2.475 g (9) Predatory Crabs 0.8 4.2 1.8 7 0.989 0.257 29.4 0.321 15.96 2X52 0.68 0.474 (10) Bivalves > 10 mm 17 34 1.2 9.9 0.872 0.121 336.6 0.152 228.5 269.3 0.848 0.179 6.723*8 2> ( 11) Suspended Scallops 14 28 I.5 9.9 0.333 0.152 277.2 0.189 179.8 221.8 0,811 0.234 6.42 z ( 12) Large Echinoderms 4.1 1 3.2 0.898 0.313 13.12 0.391 6.4 10.5 0.609 0.641 1.56 ; (13) Small Benthos < 1 cm 40 4 11.43 0.895 0.35 457*1 0.438 205.7 365.7 0.563 0.778 5.14 g (14) Macrophytes 25 0.366 - * (15) Zooplankton 0.544 0.25 18 40 160 2880 0.313 1584 2304 0.688 0.455 88 s (16) Phytoplankton 28 250 0.505 - I (17) Bacteria 5 300 600 0.316 0.5 3000 0.526 1350 2850 0.474 1.1 270 !z

Parameter values entered (in bold) and calculated by the ECQPATH II-soflware (standard). (Explanation of symbols: P/E, Q/B, EE and GE see Material and method section; FI = food intake; Net eiT. = net efficiency; R = respiration; A = assimilation). 160

Prey/predator I z 3 4 5 (1 7 s 9 111 II I.? 1.7 14 15

(I) Birds (2) Ycllotail (3) Warehow (J) Horse Mackerel 0.X (5) Small Pelagics 0.9 0.15 0.05 Il.1 0.1 0. 1 (61 Large Demersals (7) Small Demersals 0.05 ().I5 (8) Predatory snails 0. I5 0.05 0.05 0.05 0.15 (9) Predatory Crabs II.15 0.05 0.05 0.05 0.15 (IO) Bivalves > 10 mm 0.2 0.15 0.1 0.35 I). 15 ( I 1) Suspended Scallops (12) Large Echinoderms I). I II.05 0. I ( 13) Small Benthos *- I cm 0.1 0. I5 0.65 0.X 0.5 0.35 0.2 (14) Macrophytes 0. I ( 15) Zooplankton (1.95 0.9 0.2 0.05 u.05 0.7 (16) Phytoplankton 0.8 0.6 0.6s Il.' 0.95 ( 17) Bacteria 0.35 0.27 0.3 0.05

Prq -predator matrix used for the ECOPATH H-model. Numbers represent weight fractions of food ingested.

high values and the above mentioned empirical relationship is probably (at least in part) due to the fact that the macroinvertebrates mentioned are important fishing targets - their population turnover rates are thus accelerated by the fishery. The R/B estimates for the various benthic groups (1.56 to 6.72) and for the Bacteria (270) (Table 2) are near to the values given by Schwinghamer et al. (1986) (5 and 292, respectively). The respiration to assimilation ratios (R/A) for the group Predatory Snails (0.56) and for the groups Bivalves and Suspended Scallops (0.81 and 0.85) are clo SC to the values reported by Huebner & Edwards (1981) for marine carnivorous gastropods (0.28 to 0.67) and bivalves (0.57-0.79). The gross growth efficiency values (GE) calculated by the program for the groups Bivalves and Suspended Scallops (0.12, 0.15) are near the range reported for the mussel M.ytilus edulis (0.15-0.36) by Riisgard & Randlsv (1981). The GE value for the other benthic groups (between 0.26 and 0.35) lie within the range reported in the literature for macroinvertebrates (Mann, 1982). The same holds for the fish groups (0.095-0.306) (Caddy & Sharp, 1986) and for the Zooplankton. Here the GE estimate of 0.25 lies in the range of 0.17-0.30 given by Conover (1974) for Zooplankton. The changes done on the Q/B values during the modelling (from 5.5 to 4.9 for Small Demersals, from 4.70 to 5.50 for Predatory Snails. from 11.7 to 7.00 for Predatory Crabs and from 15.00 to 11.43 for Small Benthos) were rather small and the final values seem reasonable. M. Wolff/J. Exp. Mar. Biol. Ecol. 182 (1994) 149-168 161

3.2. Trophic structure, transfer ejiciencies

About half of the biomass and production is contained within the benthic domain (Fig. 2, Table 5). Benthic invertebrates comprise 47% of total system biomass (111.2 g/ m2) and have a higher food intake than the pelagic fish and bird compartments (859 g/m2 compared to 630 g/m2). Suspended scallops alone account for about 12% of total system biomass and represent 7 1 y0 of the biomass in the water column (plankton compartments not considered). The Small Benthos and the Bivalves are in terms of biomass and food intake the most prominent benthic compartments (40 g/m2 and 34 g/m2 respectively). Of the benthic predators, crabs, snails and echinoderms play a more important role than the demersal fish, not only in terms of biomass (12.5 g/m2 compared to 6 g/m2) but also in terms of food intake (65.6 g/m2 compared to 23.7 g/m2) due to the high Q/B values for crabs and snails. A significant portion of the production of the compartments Macrophytes, Zoo- plankton, Phytoplankton, Suspended Scallops is not immediately used in the system (seen by their low EE values) and enters the detritus pool, of which Bacteria use about half (3000 g/m2). A similar amount of biomass passes through the Zooplankton compartment (2880 g/m2). These two groups are far the most important “consumers” of the system. Much of the energy enters the filter feeding compartments through Bacteria (117.8 g/m2 in Bivalves, 74.8 g/m2 in Suspended Scallops, 137.1 g/m2 in the Small Benthos compartment and 144 g/m2 in Zooplankton representing 35, 27, 30 and 57; of the food of these compartments, respectively). Horse Mackerel as main zooplankton feeder contributes about 6.1 y0 to the total system biomass and consumes about 26% of the zooplankton production. Another 11 y0 is taken by the small pelagics. The biomass of large fish and birds is compara- tively small (1.8 g/m’) and their food intake, despite high Q/B ratios, rather insignifi- cant. It must be noted that the Warehoe and Yellowtail are not residents of the system, but highly migratory fish with sporadic and rather unpredictable appearance. However, the Tongoy area is the main centre of their appearance and fishery along the Chilean coast where both species occur at least during 6 months of the year (Wolff & Aron, 1991). Therefore, I considered them as characteristic elements of the system. As indicated by the model, both species are definitely not food limited. Their sporadic appearance (as yet unexplained) must thus be due to other constraints. It is possible that the temperatures, although higher in Tongoy Bay than along the open coast, are too low for a year-around presence or that these fish migrate onshore to the Tongoy Bay area prior to spawning because of the food abundance of this area. The Transfer efficiencies calculated by the ECOPATH II programm (Table 4) are very close to the 15% value proposed by Ryther (1969) for coastal zones and in the middle of the range (lo-20;/,) commonly reported in the literature (Odum, 1971; Barnes & Hughes, 1988). Fig. 3 shows a modified Lindeman pyramid, in which the volume of each trophic level compartment is proportional to the total throughput at this level (see below). Table J Tongoy Bay: transfer efficiencies for each trophic level

Sourer I 11 III IV V VI VII VIII

Producers - 13 11 13 14.7 16.2 ii.9 - Detritus 15.X 11.7 14.5 14.3 15.6 16.2 16.7 All Aous 14.2 11.4 13.9 14.4 15.7 16.’ 16.7

Proportion of total flow originating from detritus: 0.46

3.3. Ecosystem Jlow indices, summar,) statistics

The total system throughput (T), i.e. the sum of all flows (consumption, exports, respiratory flows and flows into detritus) is estimated as 20835 tjkm’lyear (Table 5) and puts the system into an intermediate position in terms of flow per area, when compared to data presented by Pauly et al. (1994). Fig. 3 shows that about 95p/, of the throughput (the “power” generated within the system - sensu Odum, 1971) is achieved from the trophic levels I to II (63%) and II to III (32.1’1;). About 529~ of it is due to consumption and fishery catches, 29:~ flows into the detritus and 19?; goes to respiration.

TROPHIC LEVEL TROUGHPUT

32,l %

63 %

Ftg. 3. Modified Lindeman pyramid of flows in the Tongoy Bay ecosystem (the volume of each discrete trophic level is proportional to the throughput (total flow) at the level. The bottom compartment represents herbivory (trophic level II). M. Wolff/J. Exp. Mar. Biol. Ecol. 182 (1994) 149-168 163

Interestingly, the T value is in the same order of magnitude, but a little lower than the value (29382) reported for the “open” Peruvian upwelling system by Jarre et al.

Table 5 Tongoy Bay

(a) Summary statistics

Sum of all consumption 7669.8 Sum of all exports 3103.3 Sum of all respiratory flows 4021.7 Sum of al flows into detritus 6040.1

Total throughput 20834.9 Sum of all production 9689.1

Fishery’s mean trophic level 3.63 Its gross efficiency (catch/net pp.) 0.0089

Total net primary production 7125 Total PP/Total R 1.772 Net system production 3 103.265 Total PP/Total biomass 30.148 Total biomass/total throughput 0.011 Total biomass (ext. Detritus) 236.3 Total catches 63.1

(b) Network flow indices

Source Ascendency Overhead Capacity

Flowbits % Flowbits % Flowbits %

Import 0 0 0 0 0 0 Internal flow 15204.6 18.8 37610.2 46.6 52814.8 65.5 Exports 5243.9 6.5 3882.4 4.8 9126.3 11.3 Respiration 5864.1 7.3 12884.5 16 18748.6 23.2

Totals 26312.6 32.6 54377.1 67.4 80689.8 100

Throughput cycled 97.5 t/km’/year Finn’s cycling index 10.1 (% of total throughput) Average path length 4.91

Percent of cycled flow through loops of various path length

Path length

2 2 3 13 4 20 5 29 6 27 7 9

(a) Summary statistics; (b) Network flow indices. For further explanations see text and Christensen & Pauly (1992). (1991) for the peak period of anchovy catches in Peru (1963-1969). The same holds true for the Ascendency/Capacity (A/C) ratio (32.69, compared to 37.44,). As this A/C ratio is presumed to be a measure of the system maturity as well as for the system’s ability to withstand perturbations (Ulanowicz, 1986) this would suggest, that the Tongoy Bay ecosystem has a somewhat higher capacity to withstand perturbations and is less mature than the open pelagic upwelling system. Another descriptor for maturity (or age) of a system is the Total Primary Production to Total Respiration ratio (PP/R) (Odum, 1971). The value calculated by the ECOPATH II software ( 1.77, Table 5) also clearly indicates that Tongoy Bay is a young inmature system. in which more energy is fixed than respired. Accordingly, the value for the net system production and the PP!B ratio is also high (Table 5). Finn’s cycling index, which gives the proportion of the flows in a system that is recycled compared with the total system throughput (Finn, 1976). is an other descriptor for system maturity (Odum, 1969). The value of 10.1 (I,, calculated for the Tongoy Bay (Table 5) is low compared with those given by Baird & Ulanowicz (1993) for four tidal estuaries which are in the range of 25-440, which also suggests a low degree of system maturity. Christensen & Pauly (1992) and Baird & Ulanowicz (1993) point out, however. that the interpretation of this index is not as simple as E.P. Odum conceived. The average path length which measures the average number of transfers a unit of flux will experience from its entry into the system until it leaves the system (Baird & Ulanowicz. 1993) is high (4.91. Table 5) when compared with the values reported for the four estuaries mentioned above (2.86-3.95). This is unexpected as it suggests a more mature system with a higher degree of connectance. in which an energy unit is retained rather long. It is interesting to note that 85”; of the cycles in Tongoy Bay involve 4 to 7 steps (Table 5), while in the four tidal estuaries mentioned above about 80”;, of the cycled flow is via short loops (path length 1 or 2) (Baird & Ulanowicz, op. cit.). Another indication for a higher degree of maturity of the Tongoy Bay ecosystem is its mean transfer efficiency (14.7”,,) which is significantly higher than for the four tidal estuaries (4.02-12.49”,) reported by the above authors. These comparisons must be taken with care, as the above authors did not use the same mode of aggregation of the living components (but a similar number of compartments. 14-16) and as they used as currency carbon (C) instead of wet weight like in the case of the Tongoy model. The mean trophic level of the Tongoy Bay fishery (3.6, about the level represented by the predatory crabs), is much higher than that reported for the Peruvian upwelling system (2.2) by Jarre et al. (op. cit.). This is due to the fact that the bay’s fishery is concentrated on primary consumers nnd a variety of species of higher trophic levels (demersal fish, predatory invertebrates, warehoe. yellowtail), whereas in the latter case, the fishery operates as an almost exclusive “anchovy predator”, The gross efficiencies for the fisheries of both systems are almost identical (0.89”,, compared to 0.9’,,). In the Tongoy Bay system. one half of the total harvest is represented by bivalves and suspended scallops and the question arises if this harvest can substantially be increased through an intensification of scallop culture. Prior to the time of hanging cultures in the bay, annual catches oscillated from about 3 t to over 400 t (SERNAP. 1978-1989). This has also occurred in other bays with important scallop banks along the SE Pacific coast. An extreme example is given by the Independence bay, located M. Wolff/J. Exp. Mar. Bid. Ecol. 182 (1994) 149-168 165

about 2000 km north of Tongoy, where during the strong El NiAo impact 1982183 scallop populations increased 60-fold and the landings rose from around 500-1000 t/ year to over 50000 t in the period subsequent to the impact (Wolff, 1987). Scallop densities of several hundred ind./m2 (equivalent to 5000 g/m2) were registered during this time (Arntz & Tarazona, 1990). At the same time, a scallop proliferation, - but of a lesser degree - was observed in Tongoy Bay (Illanes et al., 1985). One might thus assume that the capacity of the bay in terms of food for the biomass production of filter feeders (i.e. scallops) is much higher than the normally realized production. Wolff (1987,1988) states that in “normal” years the relative low standing stocks of scallops are due to recruitment bottlenecks and a high predation mortality, both significantly weakened during El N&o. To evaluate the bay’s capacity for an increased production of suspended scallops, the input data was manipulated by increasing the biomass of suspended scallops successively and the changes done by the model were registered. One clear result of this exercise is that scallop biomasses as high as those reported from Peru (> 5000 g/m2) are impossible. However, at an average scallop biomass of about 500 g/m2 (providing no other changes) the system would possibly work. Phytoplankton and Bacteria would be used more efficiently (EEs around 0.96 for both compartments) and the detritus pool would be about balanced (actually a little more is used than produced - EE > 1) Under these conditions, the gross efficiency of the fishery (harvest) would be increased by almost an order of magnitude to 7.7%; the total catch would be raised to about 549 t/km2. Under the assumption that about half of the bay’s area is suitable for scallop culture (the other half being too shallow or having too strong winds and currents) the total harvest could amount to 16 470 t (30 km2 x 549 t/km2). This is about 30% of what was naturally produced and harvested on the seafloor after El NiAo 1982/83 in the abovementioned Independence bay (Peru). At this stage, the results of the modelling exercise should be viewed as a preliminary approximation of the interactions occurring within the system. It should be stressed that some of the input values are rough estimates only. This holds especially true for the fish catch estimates that were based on the assumption that 50% of the catch stems from the Tongoy Bay area, but also for the biomass estimates for Birds and Bacteria. While an error of as much as 50% for the first group would not significantly alter the biomass budget, it would do so in case of the second group. Bacteria and probably particulate and dissolved organic matter (POM, DOM) not considered in the model are definitely crucial elements of the system. The above mentioned enormous scallop proliferations observed during El Nifio can only be explained through bacteria as food source. It remains to be elucidated what proportion of the bacteria contributing to the food of the filter feeders comes from free living water column bacteria or from detritus- associated bacteria that are periodically resuspended into the water column by tidal currents. Other shortcomings of the model are that imports and exports (apart from catches) are not known and that the diet matrix had to be assembled from quite different literature sources, of which some were of a qualitative nature. Nevertheless, I feel that the major pathways of the system are those depicted in the model (Fig. 2) and that a coherent picture of the Tongoy Bay ecosystem was obtained. 166 M. Wolff/J. Exp. Mar. Biol. Ecol. 182 (19941 149-168

It is the first model of a bay within the SE Pacific upwelling system and thus might serve as a basis for future comparisons. Obviously, further research is required to improve the input data and to verify or dismiss the results of this pilot model. Future ecological work in this bay should be multidisciplinary and should take into account that the scientific data obtained should also satisfy model requirements.

Acknowledgements

I thank Dr. V. Christensen and Dr. A. Jarre for fruitful discussions on the ECO- PATH II software system and on an earlier draft of the manuscript. I would also like to thank S. Jesse for her help with the drawings and the literature search.

References

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