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avai lab le at www.sc iencedi rec t .com

journa l homepage: www.e lsev ier .com/ locate /eco lmodel

mportance of jumbo squid Dosidicus gigas (Orbigny, 1835)n the pelagic ecosystem of the central Gulf of California

. Rosas-Luisa,∗, C.A. Salinas-Zavalaa, V. Kochb, P. Del Monte Lunac,.V. Morales-Záratea

Centro de Investigaciones Biológicas del Noroeste (CIBNOR), P.O. Box 128, La Paz, BCS 23000, MexicoUniversidad Autónoma de Baja California Sur (UABCS), Depto. de Biología Marina, P.O. Box 19-B, La Paz, BCS 23080, MexicoCentro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), P.O. Box 592, La Paz, BCS 23000, Mexico

r t i c l e i n f o

rticle history:

eceived 25 February 2008

eceived in revised form

4 June 2008

ccepted 17 June 2008

eywords:

osidicus gigas

umbo squid

a b s t r a c t

The Humboldt squid is an important predator in the pelagic ecosystem of the central Gulf

of California and the commercial catch of this species has increased over the past decade,

probable due to a decrease of several top predators (sharks, large pelagic fish and the marine

mammals) and the optimal feeding conditions in this area. Its high abundance and impor-

tant position in the pelagic food web was quantified through two trophic models of the

pelagic ecosystem of the central Gulf of California. Models represented conditions in 1980

and 2002, to document the decadal changes in ecosystem structure and function. The

models were composed of 18 functional groups, including marine mammals, birds, fish,

mollusks, crustaceans, and primary producers. Model results show direct negative effects

on principal prey groups such as myctophids and pelagic red crab and positive effects on

copath

nergy flows

cological role

sharks, marine mammals and specifically sperm whales. It thus appears that the jumbo

squid has an important role in the ecosystem and plays a central part in the overall energy

flow as main food item for most top predators, and due to its predation of organisms on

ulf of California

rophic impact

lower tropic levels.

. Introduction

he jumbo squid (Dosidicus gigas) is considered to have anmportant ecological role in pelagic ecosystems due to itsigh abundance and wide distribution (Nigmatullin et al.,001). It is preyed upon by many fish, marine mammalsnd birds and cannibalism is common (Nigmatullin et al.,001; Aguilar-Castro and Galván-Magana, 2003; Chávez-Costand Galván-Magana, 2003; Andrade-González and Galván-agana, 2003). Jumbo squid is a voracious predator that is able

o attack a great variety of prey including fish, crustaceans andther invertebrates (Ehrhardt et al., 1986; Markaida and Sosa-ishizaki, 2003). The distribution of jumbo squid is associated

∗ Corresponding author.E-mail addresses: riroluis@yahoo.com.mx (R. Rosas-Luis), csalina

delmonte@ipn.mx (P.D.M. Luna), mzarate04@cibnor.mx (M.V. Morales304-3800/$ – see front matter © 2008 Elsevier B.V. All rights reserved.oi:10.1016/j.ecolmodel.2008.06.036

© 2008 Elsevier B.V. All rights reserved.

with their principal prey, the anchovy in Chile, Peru and onthe West coast of Baja California; while in the Gulf of Califor-nia their principal prey are sardines and mackerels (Ehrhardtet al., 1986; Nevárez-Martínez et al., 2000). However recentlyMarkaida and Sosa-Nishizaki (2003), reported that the princi-pal prey are myctophids fish.

Jumbo squid has been related to the distribution of toppredators such as large pelagic sharks, sea lions, dolphins andsperm whales, among others (Klett, 1981; Jaquet and Gendron,

s@cibnor.mx (C.A. Salinas-Zavala), vokoch@uabcs.mx (V. Koch),-Zárate).

2002; Aguilar-Castro and Galván-Magana, 2003; Chávez-Costaand Galván-Magana, 2003; Andrade-González and Galván-Magana, 2003). Jumbo squid feeds at night and undertakesextensive vertical migrations, which may have an important

150 e c o l o g i c a l m o d e l l i n g 2 1 8 ( 2 0 0 8 ) 149–161

d loc

Fig. 1 – Central Gulf of California. Principal catch zone an

influence on the vertical energy flow in the ecosystem, provid-ing an efficient energy transport from the surface to deeperwaters (Klett, 1981; Markaida et al., 2005; Gilly et al., 2006).D. gigas is the only species of cephalopod with an ongoingprofitable fishery in the Gulf of California (Fig. 1). Commer-cial squid fisheries began in the early 1970s (Fig. 2), mostlysupported by small boats at a local scale. By 1980, when larger

vessels were being used, the annual catch reached more than22,000 ton. In 1982, the fishery collapsed and the squid virtu-ally disappeared for almost a decade. It reappeared since 1989and by 1993 the fishery resumed operations. Catch rapidly

Fig. 2 – Jumbo squid catch time serie

alization of jumbo squid “Santa Rosalia and Guaymas”.

increased to 140,000 ton in 1997. During the 1997–1998 fish-ing season an extraordinary relocation of the fishing groundstook place. Ehrhardt et al. (1986) stated that during Febru-ary and March of normal years, the squid migrates towardsthe central gulf where it remains concentrated for at leastthe spring season. During 1997–1998, however landing recordsfrom Guaymas and Santa Rosalia the most important fishing

harbors inside the Gulf indicated almost no catch during thosemonths, while high concentrations of squid were detectedoff the west coast of the peninsula. During the last yearssquid became one of the most important fisheries in the

s in Baja California Sur, Mexico.

e c o l o g i c a l m o d e l l i n g 2 1 8 ( 2 0 0 8 ) 149–161 151

Table 1 – Input values for the mass balanced model of the central portion of the Gulf of California

Group Biomass (ton/km2) P/B per year Q/B per year EE

1 Sea birds 0.01 (5) 0.38 (10) 73.8 (10)2 Sperm whale 0.03 (11, 15)a 0.03 (17) 5.27 (11)b

3 Marine mammals 0.02 (5) 0.08 (10) 20.3 (10)4 Pelagic shark (21) 0.47 (5) 7.63 (5) 0.745 Large pelagic fish 0.19 (16, 19) 1.26 (16) 9.75 (4, 20)c 0.76 Medium pelagic fish 1.11 (3) 0.88 (14) 5.2 (14) 0.967 Small pelagic fish 5.74 (10) 4.5 (14) 15.7 (14) 0.948 Demersal fish 1.79 (14) 0.96 (9) 3.78 (9) 0.879 Myctophidae 0.86 (14) 1.59 (14) 7.26 (14) 0.8

10 Jumbo squid 0.57 (12) 3.25 (8, 12)d 13.8 (2)e

11 Euphausids 1.1a 7 (7) 24.9e

12 Pelagic red crab 2.7 (1) 1.2 (6) 17.4 (14)13 Macrobenthic invertebrates 0.83 (14) 3.48 (9) 12.7 (9) 0.914 Shrimps 0.59 (14, 18) 2.29 (18) 26.2 (10)15 Zooplankton 12 (5) 25.68 (14) 86.3 (14) 0.916 Meiobenthos 2.11 (14) 11.28 (9) 39.5 (9)17 Phytoplankton 95.95 (5) 0.918 Detritus 3 (5)

Jumbo squid biomass in 1980 was 0.99 ton/km2. Sources of input values are shown next to the value. Sources of information correspondingto numbers: (1) Mathews et al. (1975); (2) Klett (1981); (3) Pérez-Mellado and Findley (1985); (4) Ehrhardt (1991); (5) Martínez-Tortolero (1994); (6)Balart (1996); (7) Gómez et al. (1996); (8) Klett (1996); (9) Godínez-Domínguez et al. (1999); (10) Pérez-Espana (1999); (11) Clarke and Paliza (2000);(12) Nevárez-Martínez et al. (2000); (13) Markaida-Aburto (2001); (14) Arreguín-Sánchez et al. (2002); (15) Jaquet et al. (2003); (16) Macias-Zamora(2003); (17) Olson and Watters (2003); (18) Morales-Zárate et al. (2004); (19) INP (2004); (20) FISHBASE; (21) estimated by Ecopath.a Mean weight × number of organisms (standardized to m2).b Consumption/biomass.c ln(Q/B) = −0.178 − 0.202 ln W∞ + 0.612 ln T + 0.516 ln A + 1.26F.

coah(p1enMe2

tsouflatapfbbtlif

d P = B/42e(5.21 − 0.752 ln t).e Q = (R + P)/(EA).

ountry and probably the most dramatic case of a widelyscillating fishery in the Gulf of California (Lluch-Cota etl., 2007). The causes of this variability are unknown, butypotheses range from hydrographic and biological processes

migratory responses of mainly small pelagic populations torey availability, reproductive success and recruitment: Klett,981; Ehrhardt et al., 1982, 1986). However there is strongvidence that ENSO event is the strongest interannual sig-al influencing the system and also jumbo squid (Robles andarinone, 1987; Marinone, 1988; Lavín et al., 2003; Bazzino

t al., 2007; Herrera-Cervantes et al., 2007; Lluch-Cota et al.,007).

Due to its abundance, feeding behavior and its impor-ance as a fishery resource, jumbo squid is an importantpecies in the food web of the pelagic ecosystem in the Gulff California. Changes in its abundance may influence pop-lation size and distribution of its predators and the energyow patterns and function of the pelagic ecosystem (Cury etl., 2000; Menge, 2000; Achá and Fontúrbel, 2003). Thereforehe objective of this study was to determine the importancend function of the jumbo squid in the tropic flows of theelagic ecosystem in the central portion of the Gulf of Cali-ornia, through the implementation of two trophic models ofiomass flows (Christensen and Pauly, 1993). One model wasuild for the year 1980 when squid fishery was incipient and

he other for the year 2002 when the fishery was well estab-ished. In this way we could compare the ecosystem takingnto account the different abundance of jumbo squid as a mainactor.

2. Materials and methods

2.1. Description of Ecopath trophic flow model

The balance of biomass flows in the Ecopath type models isdescribed by simple linear equations (Polovina and Ow, 1983;Polovina, 1984; Christensen and Pauly, 1992; Christensen et al.,2002) and they are basically expressed as follows:

Bi

(P

B

)iEEi −

n∑j=1

Bj

(Q

B

)jDCji − Yi − Ei − BAi = 0 (1)

where B = biomass (i prey, j predator; functional group given),P/B = production/biomass, proportion which equals to theinstant total rate of mortality (Z), in a condition of bal-ance (Allen, 1971), EEi = ecotrophic efficiency which representsthe fraction of production either consumed or fished fromthe system, (Q/B)j = biomass/group consumption j, DCji = groupfraction i in the predators diet j. Yi is the total fishery catch rateof (i). Ei the net migration rate. BAi is the biomass accumulationrate for (i).

Eq. (1) represents the balance in the group’s biomass iin the ecosystem. Every group are represented by a similarequation, these simultaneous linear equations are solved byusing matrix algebra (Walter, 1979). The groups in the model

are represented by these equations and trophic interactionsbetween groups are described by a diet matrix that quanti-tatively describes the fractions that each group has in eachothers groups diet.

i n g

152 e c o l o g i c a l m o d e l l

Construction of the pelagic ecosystem model in the centralportion of the Gulf of California for 1980 and 2002.

A total of 18 representative functional groups were selectedeach of them integrated by one or several species with a simi-lar trophic role within the ecosystem. Out of the 18 functionalgroups (Table 1), one is a primary producer, one stands fordetritus, one for zooplankton, six invertebrates, five for bonyfish, one for cartilaginous fish, two for marine mammals andone for sea birds. Sperm whale (Physeter macrocephalus), jumbosquid (D. gigas) and the pelagic red crab (Pleuroncodes planipes)were treated individually as they are of particular interestfor this study. For each functional group, input parameters(biomass, mortality, production/biomass P/B, ecotrophic effi-ciency EE, diet composition and food intake, and fishery data)were taken from the available literature (see Table 1) and stan-dardized to units of ton km−2 year−1.

For the 1980 simulation modifications were made only indiet and biomass of jumbo squid group. Due to the absenceof verified data of other group parameters two assumptionswere made:

(1) The P/B, Q/B and EE values from all the functional groupsare the same for both years 1980 and 2002.

(2) The nutritional regimen for the functional groups was thesame for both models as there is no reliable data of dietfor the 1980 groups, with the exception of jumbo squid.

2.2. Biomass

Biomass values were compiled from information reported indifferent studies form the area (Table 1). Jumbo squid biomassin 1980 was estimated in 0.99 ton/km2 in the Gulf of California(Ehrhardt et al., 1986).

Biomass values for sperm whales and euphausids for the2002 model were calculated by using Eq. (2), considering abun-dance reported by Clarke and Paliza (2000) and Jaquet et al.(2003) for the sperm whale, and by Lavaniegos et al. (1989) foreuphausids.

B = average weight(organism number × area km2) (2)

Due to the lack of information, the biomass value forpelagic sharks was calculated by the Ecopath model.

2.3. P/B relation

P/B relations were obtained from the literature cited in Table 1.For jumbo squid and euphausids the P/B values were calcu-lated by using Eq. (3) (Kavanagh, 2002):

P =(

B

42

)e(5.21−0.752 ln t) (3)

where t = life span in years, which in euphausids 1 year and itis known as 2 years length of life for jumbo squid.

2.4. Q/B relation

The Q/B relation refers to the amount of food consumed perunit of biomass over a certain period of time. Values for bony

2 1 8 ( 2 0 0 8 ) 149–161

fish groups were obtained from Arreguín-Sánchez et al. (2002)with the exception of the large pelagic groups for which valueswere taken from FISHBASE, Ehrhardt (1991) and the followingequation (Palomares and Pauly, 1989):

ln(

Q

B

)= −0.178 − 0.202 ln W∞ + 0.612 ln T + 0.516 ln A

+1.26F (4)

where W∞ = maximum asymptotic weight, gotten from thegrowth curve of von Bertalanfy, T = average temperature of thehabitat in ◦C, A = aspect ratio of the fin = h2/s (h is the heightand s the surface area of the fin), F = type of nutrition (0 forcarnivorous, 1 for herbivorous and 0.5 for omnivorous)

The value of Q/B for the sperm whale group was obtained bydividing the consumption reported by Clarke and Paliza (2000)by the sperm whale biomass in the area; for the squid datawas taken from Klett (1981) and Markaida-Aburto (2001) usingthe following equation (Kavanagh, 2002):

Q = R + P

EA(5)

where R = rate of breathing in ml O2 (individually h)−1,R = 7.0W0.75 (W is the individual weight with �g of dry weight),P = production, EA = assimilation efficiency using a value of80% for animals.

2.5. Ecotrophic efficiency

One of the basic assumptions of steady state models isthat the terms of the equations balance out. The programcalculates the ecotrophic efficiency. But for nine groups(pelagic sharks, large pelagic fish, medium pelagic fish, minorpelagic fish, demersal fish, myctophids, macrobenthic inver-tebrates, zooplankton and phytoplankton) the values reportedby Arreguín-Sánchez et al. (2002) were used (Table 1).

2.6. Fisheries

Catch time series for large, medium and small pelagic fish,pelagic sharks, demersal fish and shrimp were taken from theAnuario estadistico de pesca (2002). For squid they were takenfrom landing data provided by the fisheries office in SantaRosalia B.C.S. and Guaymas in Sonora for 2002. The capturevalues used in the 1980 model, were taken from Casas-Valdezand Ponce-Díaz (1996) for pelagic sharks, large and mediumpelagic fish; Ehrhardt et al. (1980) for demersal fish, Ehrhardtet al. (1986) for jumbo squid, De Anda et al. (1994) for smallpelagic fish and from Margallon (1987) and López et al. (2000)for shrimp, all values are reported in Table 2.

2.7. Diet matrix

Diet composition of the different functional groups in 2002was estimated based on the reported studies of stomach con-

tent analysis. The citations are listed in Table 3 where also theproportion of each prey group in the diet is shown. For thesimulation of the system in 1980 the diet composition for thejumbo squid was taken from Ehrhardt et al. (1986) (Table 3).

e c o l o g i c a l m o d e l l i n g 2 1 8 ( 2 0 0 8 ) 149–161 153

Table 2 – Catch by group in the central portion of the Gulf of California for both models (ton km−2 year−1)

Group Minor ships Mayor ships Both

1980 2002 1980 2002 1980 2002

Pelagic shark 0.02 0.03Large pelagic fish 0.06 0.1Medium pelagic fish 0.01 0.01Small pelagic fish 0.67 0.56

2

Tsdnmtaata

E1ib3mtnafl

2

Tt

T

wj

3

3G

T1aewt

Demersal fishJumbo squid 0.02 0.28Shrimps

.8. Balance, calibration and validation of the models

he models were balanced by adjusting the input parameterso that EE values were <1. This was achieved by adjusting theiet matrix observing that the changes in diet composition didot exceed 1%. Only groups, for which no detailed diet infor-ation was available, were modified. The balanced model was

hen checked whether some of the output parameters suchs respiration/biomass ratio R/B, were within reported limits,s they are higher in more active and endothermic organismhan for ectothermic and/or sedentary groups (Christensennd Pauly, 1993; Christensen et al., 2002).

Calibration and validation of the model was done with thecoranger routine, using 10,000 runs (Pauly and Christensen,996). Ecoranger tries to optimize the model through minimiz-ng the residuals. Ecoranger uses an algorithm semibayesianased on the Montecarlo method, by defining a minimum of0% of positive runs as a limit of acceptance of the balancedodel. On previous software versions, this routine modified

he values of P/B, Q/B and the diet matrix. In the present study,o diet matrix values were modified in the Ecoranger routines this was considered the core data for the systems trophicows.

.9. Trophic characterization of the system

he trophic level was calculated for each functional grouphrough:

L = 1 +n∑ji

DCji × TLj (6)

here TL = trophic level of the group, TLj = trophic level of prey, DCji = proportion of prey j in the predators diet.

. Results

.1. Attributes of the pelagic ecosystem of the centralulf of California

he Ecoranger routine gave a total of 56% of positive runs for980 and 54% for 2002 and the balanced model was therefore

ccepted. The values calculated by the program for both mod-ls (1980 and 2002) are given in Table 4. All of the EE valuesere below 1, and there was a tendency of EE to diminish as

ropic level increases. The lowest EE values belong to marine

0.06 0.090.02 0.110.2 0.12

birds, sperm whale, marine mammals, but also to the pelagicred crab (Table 4).

The biomass of the groups that from part of the diet of D.gigas was higher in 1980 than in 2002. The group with the high-est increase was the pelagic red crab that changed from 2.7 to8.9 ton/km2 in 2002. Biomass of medium pelagic fish dimin-ished from 5.7 to 2.1 ton/km2 and for small pelagic fish from 1.1to 0.79 ton/km2. Biomass of the most top predators increasedfrom 1980 to 2002 model. Only the sperm whale group showeda decrease from 0.32 ton/km2 in 1980 to 0.03 ton/km2 in 2002(Table 4). For pelagic sharks, the model produced a biomassestimate of 0.08 ton/km2 for 2002, higher than the 1980 esti-mate (Table 4).

The higher R/B values generally belonged to the groupswith small organisms at lower trophic levels. However, seabirds had the highest value of 58.6 in both models followedby zooplankton with a value of 43.3. The R/B value for thejumbo squid group was 7.8 (Table 4). Respiratory/assimilation(R/A) ratios were between 0.63 and 0.99, with the highervalues at the upper trophic levels. Jumbo squid and myc-tophids showed values above the average (0.71 and 0.73,respectively). Regarding the omnivory index, the lowest val-ues belonged to meiobenthos (0.05), the highest values werefound in myctophids (0.35), followed by macrobenthic inver-tebrates (0.33). The value for the jumbo squid group was low0.09 (Table 4).

3.2. Trophic characterization

The ratio for the total primary production/total respira-tion (TPP/TR) (Table 5) was 1.08 in 1980 and 1.3 for 2002.The value of total primary production/total biomass for1980 model was 16.96, less than the 2002 value with 23.71.The systems total capacity was smaller in 1980 with 8341 ton km−2 year−1 compared to 9 569 ton km−2 year−1 in 2002(Table 6). The capacity of jumbo squid presented a value of121.47 ton km−2 year−1 in 1980, while in 2002 the value wasonly 80.16 ton km−2 year−1. The sperm whale in 1980 pre-sented a value of 18.53 ton km−2 year−1, eight times larger thanthe 2.3 ton km−2 year−1 from 2002. The ascendency (A) for 1980was 1957 flowbits (A = 2512 flowbits for 2002) representing 23%(26% for 2002) of the total system capacity, and the overhead(O) was 76.6% (6383 flowbits; and for 2002 O = 7056 flowbits or73%) and thus the ascendency/capacity ratio was 0.23 and 0.26,

respectively.

Fig. 3 shows the Ecopath results representing the directand indirect impacts among groups in the system. In the1980 simulation the jumbo squid was positively affecting the

154e

co

lo

gic

al

mo

de

ll

ing

21

8(2

00

8)

149–161

Table 3 – Diet matrix for central portion of the Gulf of California model in 2002, the same data were used in the 1980 model, except for D. gigas in parenthesis

Prey/predator 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

1. Sea birds2. Sperm whale3. Marine mammals4. Pelagic shark5. Large pelagic fish 0.046. Medium pelagic fish 0.1 0.1 0.11 0.43 0.25 0.027. Small pelagic fish 0.53 0.35 0.15 0.34 0.32 0.16 0.09 (0.37)8. Demersal fish 0.14 0.17 0.05 0.11 0.01 0.02 (0.1)9. Myctophidae 0.13 0.57 (0.09)10. Jumbo squid 0.12 0.69 0.13 0.22 0.1 0.04 (0.08)11. Euphausids 0.11 0.1 0.05 (0.17)12. Pelagic red crab 0.09 0.03 (0.03)13. Macrobenthic invertebrates 0.21 0.11 0.11 0.11 0.02 0.18 (0.12) 0.0514. Shrimps 0.0715. Zooplankton 0.12 0.24 0.42 0.86 0.1 0.59 0.3 0.17 0.15 0.1616. Meiobenthos 0.18 (0.04) 0.09 0.31 0.0517. Phytoplankton 0.14 0.06 0.36 0.3 0.17 0.14 0.18 0.7818. Detritus 0.02 0.21 0.03 0.4 0.66 0.57 0.51 0.06 0.95

Sum 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

Sources of information corresponding to number groups: (1, 3) Hernandez-Herrera and Cisneros-Mata (1999); (2) Clarke and Paliza (2000) and Ruiz-Cooley et al. (2004); (4) Aguilar-Castro and Galván-Magana (2003), Chávez-Costa and Galván-Magana (2003), and Andrade-González and Galván-Magana (2003); (5) INP (2004), Abitia-Cárdenas et al. (1999), Abitia-Cárdenas et al. (2002), and Rosas-Aloyaet al. (2002); (6) Konchina (1983), Díaz-Gonzáles and Soto (1988), and Chávez-Solano (1976); (7, 9, 13) Arreguín-Sánchez et al. (2002); (8) Langton and Bowman (1981); (10) Markaida-Aburto (2001); (11)Lavaniegos et al. (1989); (12) Pérez (1991); (14, 16) Godínez-Domínguez et al. (1999); (15) Pérez-Espana (1999).

ec

ol

og

ica

lm

od

el

lin

g2

18

(20

08

)149–161

155

Table 4 – Input and estimated values (in bold) for the central portion of the Gulf of California models

Group Trophic level Biomass P/B peryear

Q/B peryear

EE P/Q R/B peryear

Assimilation(ton km−2 year−1)

R/A(ton km−2 year−1)

P/R(ton km−2 year−1)

Flux to detritus(ton km−2 year−1)

Omnivoryindex

1980 2002 1980 2002 1980 2002 1980 2002 1980 2002

Sea birds 4.08 4.07 0.01 0.01 0.38 73,77 0.01 0.005 58.64 0.61 0.77 0.99 0.01 0.16 0.2 0.16 0.15Spermwhale

4.48 4.44 0.32 0.03 0.03 5.27 <0.00 0.006 4.19 1.35 0.13 0.99 0.01 0.35 0.03 0.29 0.27

Marinemammals

4.01 4 0.01 0.01 0.08 20.25 0.05 0.004 16.12 0.19 0.24 0.99 0.01 0.05 0.06 0.24 0.23

Pelagicshark

4.39 4.38 0.06 0.08 0.47 7.63 0.73 0.06 5.63 0.37 0.49 0.92 0.08 0.1 0.13 0.19 0.18

Largepelagicfish

4.1 4.09 0.09 0.19 1.26 9.75 0.7 0.13 6.54 0.67 1.52 0.84 0.19 0.2 0.45 0.21 0.2

Mediumpelagicfish

3.52 0.79 1.11 0.88 5.2 0.96 0.17 3.27 3.3 4.61 0.79 0.27 0.85 1.19 0.2

Smallpelagicfish

3.03 2.17 5.74 4.5 15.72 0.94 0.29 8.07 27.24 72.22 0.64 0.56 7.4 19.61 0.17

Demersalfish

3.11 2.13 1.79 0.96 3.78 0.87 0.25 2.07 6.44 5.42 0.68 0.46 1.88 1.58 0.45

Myctophidae 2.74 1.49 0.86 1.59 7.26 0.8 0.22 4.22 8.64 5.01 0.73 0.38 2.63 1.52 0.35Jumbosquid

3.79 3.74 0.99 0.57 3.25 13.82 0.68 0.23 7.8 10.9 6.28 0.71 0.42 3.74 2.16 0.16 0.09

Euphausids 2.36 1.04 1.1 7 24.89 0.75 0.28 12.91 20.7 21.9 0.65 0.54 6.99 7.4 0.3Pelagicred crab

2.2 8.91 2.7 1.2 17.36 0.13 0.07 12.69 123.81 37.5 0.91 0.09 40.29 12.2 0.2

Macrobenthicinverte-brates

2.45 1.32 0.83 3.48 12.7 0.91 0.27 6.68 13.46 8.46 0.66 0.52 3.79 2.38 0.33

Shrimps 2.33 0.81 0.59 2.29 26.2 0.75 0.09 18.67 16.95 12.36 0.89 0.12 4.7 3.43 0.24Zooplankton 2.19 7.77 12 25.68 86.26 0.9 0.3 43.33 536.49 828.13 0.63 0.59 154.08 237.9 0.19Meiobenthos 2.05 2.69 2.11 11.28 39.52 0.52 0.29 20.33 93.55 66.8 0.64 0.55 39.55 28.24 0.05Phytoplankton1 6.63 9.76 95.95 0.9 63.62 93.69 0Detritus 1 3 3 0.48 0 0.31 0.34

Left panel shows main ecological attributes.

156 e c o l o g i c a l m o d e l l i n g 2 1 8 ( 2 0 0 8 ) 149–161

Table 5 – Summary statistics of the pelagic ecosystem in the central portion of the Gulf of California

Parameter Value 1980 Value 2002 Units

Sum of all consumption 1080.87 1339.82 ton km−2 year−1

Sum of all exports 47.12 215.79 ton km−2 year−1

Sum of all respiratory flows 589.02 692.61 ton km−2 year−1

Sum of all flows into detritus 330.38 412.13 ton km−2 year−1

Total system throughput 2047 2660 ton km−2 year−1

Sum of all production 912 1316 ton km−2 year−1

Mean tropic level of the catch 3.01 3.3Gross efficient (catch/net totally production 0.001 0.001Calculated total net primary production 636.16 936.91 ton km−2 year−1

Total primary production/total respiration 1.08 1.35Net system production 47.14 244.30 ton km−2 year−1

Total primary production/total biomass 16.96 23.71Total biomass/total throughput 0.02 0.01Total biomass (excluding detritus) 37.50 39.51 ton/km2

1.050.270.225

Total catchConnectance indexSystem omnivory index

sperm whale and pelagic shark groups, while it was negativelyaffecting pelagic red crabs, myctophids, demersal fish andminor pelagic fish due to the predation. Negative effects onlarge pelagic fish and marine mammals were indirect throughcompetition. There was a negative fishing impact on sharks,minor pelagic fish and demersal fish in both years, withoutfinding any effects on jumbo squid. Jumbo squid predationshowed a major impact on the minor pelagic fish, demersalfish, myctophids, pelagic red crab, macrobenthic invertebratesand euphausids in 1980 being modified in 2002, where a majordepredation was observed on myctophids fish, euphausids,

pelagic red crab and macrobenthic invertebrates (Table 7).

In both years fishing caused a negative impact on pelagicshark and the impact was higher in 2002 by the increase ofthis activity since 1980 (Table 2, Fig. 3). The fisheries impacts

Table 6 – Flux index for the central portion of the Gulf of Califor

Group 1980

Ascendency Overhead

Sea birds 0.94 8.29Sperm whale 2.09 16.45Marine mammals 0.29 2.93Pelagic shark 0.54 5.61Large pelagic fish 1.03 9.53Medium pelagic fish 7.65 36.18Small pelagic fish 53.97 216.31Demersal fish 12.76 65.54Myctophidae 16.20 82.24Jumbo squid 21.37 100.11Euphausids 32.48 179.99Pelagic red crab 180.37 535.39Macrobenthic invertebrates 24.41 126.17Shrimps 24.52 140.28Zooplankton 250.19 2155.83Meiobenthos 116.06 565.40Phytoplankton 615.91 1101.03Detritus 596.70 1036.22Total 1957.47 6383.54(%) 23.47 76.53

Values are in ton km−2 year−1 bits.

1.29 ton km−2 year−1

0.280.216

in other groups were highest in the demersal fish and minorpelagic fish groups.

4. Discussion

The total system throughput increased by 23% from 1980 to2002 (2047 and 2660 ton km−2 year−1), well within the rangefound in other systems that include squid and cephalopodsas functional groups (Alino et al., 1993; Mendoza, 1993; Schalket al., 1993; Olson and Watters, 2003; Arancibia and Neira,

2003). However they are below the values reported in for-mer models of the Gulf of California (Arreguín-Sánchez et al.,2002: 4 224 ton km−2 year−1 and Morales-Zárate et al., 2004:6 633 ton km−2 year−1). The main reason is probably that for-

nia model

2002

Capacity Ascendency Overhead Capacity

9.23 1.31 10.36 11.6718.54 0.22 2.12 2.343.22 0.41 3.79 4.206.15 0.72 7.27 8.00

10.56 2.13 19.51 21.6543.83 11.42 49.99 61.41

270.28 75.44 398.47 473.9178.31 8.02 54.71 62.7398.44 40.08 61.08 101.16

121.48 10.95 69.21 80.16212.47 33.54 196.68 230.23715.76 60.75 254.80 315.56150.58 23.01 89.89 112.90164.80 20.35 112.64 132.99

2406.01 490.51 2823.40 3313.91681.46 101.39 457.42 558.81

1716.94 834.39 1311.81 2146.201632.93 798.25 1133.69 1931.958341.00 2512.90 7056.87 9569.76

100 26.26 73.74 100

e c o l o g i c a l m o d e l l i n g 2 1 8 ( 2 0 0 8 ) 149–161 157

Fig. 3 – Mixed trophic impact groups of the central portion of the Gulf of California in 1980 (right) and 2002 (left), blacki

mAafluipg

wcsstNaidmtaaa

moljttsgTjo

ndicates positive and gray negative impact.

er models consisted of about 50% more groups (27 groups inrreguín-Sánchez et al., 2002, 29 groups in Morales-Zárate etl., 2004, compared to 18 in this study), which increases totalow, due to the larger amount of trophic interactions. Howeversing a lot of groups in a trophic model cause a considerable

ncrease of error, because many of the input data is not veryrecise, therefore we decided to rather keep the number ofroups small, sacrificing detail for the sake of precision.

The ecosystem was more developed in 1980 than in 2002ith regard to values of P/R, P/B, and net production of the

ommunity and it changed to a state of lesser organization,tability and resilience according to the trend of the relativeystem ascendency (A/C) which are indicators of ecosys-em maturity (Odum, 1969; Ulanowicz, 1986; Ulanowicz andorden, 1990; Christensen, 1995; Muller, 1996; Christensennd Walters, 2004). The lower development of the ecosystemn 2002 can be probably explained by the decrease in abun-ance of the top predators reflecting a worldwide trend inarine food webs that causes changes in the trophic flow pat-

erns and the development of the system due to the decreasingbundance of predators that minimizes predation (Hairston etl., 1960; Begon et al., 1990; Rinaldi, 1994; Heikkila, 1997; Caddynd Rodhouse, 1998).

The model results identified the jumbo squid as one of theost important predators, with a trophic level of 3.79 (Table 4),

nly 14.6% less than the sperm whales which is the highestevel predator in the system. Comparatively, the biomass ofumbo squid is higher than the other groups (280% more thanhe large pelagic fish, which is the most abundant predator inhis system in 2002). With this, the effects caused by jumboquid in the ecosystem are remarkable within the predator

roups in which the competition for food increases (Table 7).he decreasing abundance of its predators may have caused

umbo squid abundance to increase, which has already beenbserved in several ecosystems where the fish groups are the

only ones that compete with squid (Alino et al., 1993; Sambilay,1993; Schalk et al., 1993).

Jumbo squid is a key species within the pelagic ecosys-tem of the Gulf of California. Its high abundance, high foodintake and production and its great importance as predatorand prey suggest that is a very important element for energytransfer within the food web. This is reflected by its impact onsmall pelagic fish (Fig. 3), as jumbo squid may affect this groupduring their migrations into the Gulf of California (Ehrhardt,1991). However jumbo squid can easily change its prey ashappened in the 2002 model, where myctophids were theirmain prey item (Fig. 3). Apparently, jumbo squid is to a largedegree opportunistic, switching their diet readily when preyabundance and composition change in the area (Klett, 1981;Markaida and Sosa-Nishizaki, 2003).

The sperm whale is one the most important predator thatincreased its biomass according to increasing of jumbo squidbiomass and probably because jumbo squid being the mainfood item of sperm whales (70% of their diet). The patternsof this trophic relation (sperm whale–jumbo squid) have beenobserved in other ecosystems where jumbo squid is present. Inthe Humboldt current the sperm whale population decreasedafter jumbo squid overfishing in the 1980s (Clarke et al.,1992, 1993), this relation is not clear in the Gulf of Califor-nia, apparently the jumbo squid biomass declined in 1982,then 1989 jumbo squid biomass began to increase, but it didnot exceed the value of 1980 (0.32 ton/km2). Sperm whalehas been increasing since the same time (Gendron, personnelcommunication, 2005), probably in response to jumbo squidabundance and that sperm whale is not being fished anymore.

There is evidence that jumbo squid plays a significant part

in the regulation of trophic flows in this system and that itmust be considered an important predator in the system likesharks and marine mammals. As top predators diminishedworld wide, cephalopod biomass increases and they assume

158 e c o l o g i c a l m o d e l l i n g

Tabl

e7

–C

onsu

mp

tion

per

cen

tage

ofth

ep

rin

cip

alp

red

ator

inth

eG

ulf

ofC

alif

orn

iain

1980

and

2002

,val

ues

are

rem

ark

wh

enju

mbo

squ

idis

the

mos

tim

por

tan

tco

nsu

mer

Sea

bird

sSp

erm

wh

ale

Mar

ine

mam

mal

sPe

lagi

csh

arks

Larg

ep

elag

icfi

shM

ediu

mp

elag

icfi

shM

inor

pel

agic

fish

Dem

ersa

lfi

shM

ycto

ph

idae

Jum

bosq

uid

Det

ritu

s

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

1980

2002

Med

ium

Pela

gic

fish

3.50

0.73

1.50

11.9

121

.60

6.78

53.9

8M

inor

pel

agic

Fish

2.62

2.13

0.52

0.43

0.44

0.37

1.80

2.62

8.32

7.50

8.10

4.40

31.7

02.

9646

.50

79.5

8D

emer

salfi

sh2.

935.

921.

122.

330.

641.

352.

719.

822.

233.

0538

.03

6.68

52.3

470

.85

Myc

top

hid

ae11

.92

11.1

730

.08

66.2

658

.00

22.5

7Ju

mbo

squ

id1.

533.

7419

.76

3.60

0.51

1.29

1.73

4.36

1.39

6.08

11.5

59.

5963

.53

71.3

4Eu

ph

ausi

ds

0.18

0.22

0.18

0.23

3.48

4.59

11.7

629

.46

6.46

5.15

2.60

1.43

19.1

52.

7456

.18

56.1

8Pe

lagi

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ab0.

181.

363.

111.

9396

.71

96.7

2M

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inve

rteb

rate

s4.

450.

570.

641.

171.

143.

5714

.14

16.5

32.

712.

1818

.80

25.2

958

.12

50.7

0

r

2 1 8 ( 2 0 0 8 ) 149–161

the role of top predators in the respective ecosystems (Caddyand Rodhouse, 1998), and in the Gulf of California this effecthas been observed. Jumbo squid is affecting the biomass anddistribution of its preys and by compete to predators.

It thus appears that the ecological role of D. gigas willbecome more important over time, principally since the1990s. We only obtained this conclusion with modification injumbo squid biomass, the only one estimation of jumbo squidbiomass in the pas was made for Ehrhardt et al. (1986) andthis was higher than the 2002 estimation (Nevárez-Martínezet al., 2000). We know that ecosystem is changing year to yearas jumbo squid biomass, therefore the jumbo squid biomasschanged from 1980 to 1982 with a drastic collapse. It reap-peared since 1989, when both feeding competition and itspredation have diminished for jumbo squid. Thus, in futuremodel scenarios, we would expect that jumbo squid plays aneven more important role in regulating energy flow patternsin the pelagic ecosystem of the central Gulf of California. Thismust be taken into account when considering managementof the jumbo squid fishery in particular, and ecosystem man-agement and conservation in general.

Acknowledgements

The authors thank to Marco Medina of ideas of this work,Centro de Investigaciones Biológicas del Noroeste S.C. andCephalopods Group by commentaries and support. PdMLthanks COFAA and EDI of the IPN for financial support.

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