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

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Importance of jumbo squid Dosidicus gigas (Orbigny, 1835) in the pelagic ecosystem of the central Gulf of California R. Rosas-Luis a,∗ , C.A. Salinas-Zavala a , V. Koch b , P. Del Monte Luna c , M.V. Morales-Zárate a a b c

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

a r t i c l e

i n f o

a b s t r a c t

Article history:

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

Received 25 February 2008

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

Received in revised form

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

14 June 2008

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

Accepted 17 June 2008

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

Keywords:

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

Dosidicus gigas

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

Jumbo squid

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

Ecopath

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

Energy flows

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

Ecological role

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

Gulf of California

lower tropic levels.

Trophic impact

1.

Introduction

The jumbo squid (Dosidicus gigas) is considered to have an important ecological role in pelagic ecosystems due to its high abundance and wide distribution (Nigmatullin et al., 2001). It is preyed upon by many fish, marine mammals and birds and cannibalism is common (Nigmatullin et al., ˜ 2003; Chávez-Costa 2001; Aguilar-Castro and Galván-Magana, ˜ and Galván-Magana, 2003; Andrade-González and Galván˜ 2003). Jumbo squid is a voracious predator that is able Magana, to attack a great variety of prey including fish, crustaceans and other invertebrates (Ehrhardt et al., 1986; Markaida and SosaNishizaki, 2003). The distribution of jumbo squid is associated

∗

© 2008 Elsevier B.V. All rights reserved.

with their principal prey, the anchovy in Chile, Peru and on the West coast of Baja California; while in the Gulf of California their principal prey are sardines and mackerels (Ehrhardt et al., 1986; Nevárez-Martínez et al., 2000). However recently Markaida and Sosa-Nishizaki (2003), reported that the principal prey are myctophids fish. Jumbo squid has been related to the distribution of top predators such as large pelagic sharks, sea lions, dolphins and sperm whales, among others (Klett, 1981; Jaquet and Gendron, ˜ 2003; Chávez-Costa 2002; Aguilar-Castro and Galván-Magana, ˜ and Galván-Magana, 2003; Andrade-González and Galván˜ 2003). Jumbo squid feeds at night and undertakes Magana, extensive vertical migrations, which may have an important

Corresponding author. E-mail addresses: [email protected] (R. Rosas-Luis), [email protected] (C.A. Salinas-Zavala), [email protected] (V. Koch), [email protected] (P.D.M. Luna), [email protected] (M.V. Morales-Zárate). 0304-3800/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.ecolmodel.2008.06.036

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Fig. 1 – Central Gulf of California. Principal catch zone and localization of jumbo squid “Santa Rosalia and Guaymas”.

influence on the vertical energy flow in the ecosystem, providing an efficient energy transport from the surface to deeper waters (Klett, 1981; Markaida et al., 2005; Gilly et al., 2006). D. gigas is the only species of cephalopod with an ongoing profitable fishery in the Gulf of California (Fig. 1). Commercial squid fisheries began in the early 1970s (Fig. 2), mostly supported by small boats at a local scale. By 1980, when larger vessels were being used, the annual catch reached more than 22,000 ton. In 1982, the fishery collapsed and the squid virtually disappeared for almost a decade. It reappeared since 1989 and by 1993 the fishery resumed operations. Catch rapidly

increased to 140,000 ton in 1997. During the 1997–1998 fishing season an extraordinary relocation of the fishing grounds took place. Ehrhardt et al. (1986) stated that during February and March of normal years, the squid migrates towards the central gulf where it remains concentrated for at least the spring season. During 1997–1998, however landing records from Guaymas and Santa Rosalia the most important fishing harbors inside the Gulf indicated almost no catch during those months, while high concentrations of squid were detected off the west coast of the peninsula. During the last years squid became one of the most important fisheries in the

Fig. 2 – Jumbo squid catch time series in Baja California Sur, Mexico.

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

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Group

Biomass (ton/km2 )

Sea birds Sperm whale Marine mammals Pelagic shark Large pelagic fish Medium pelagic fish Small pelagic fish Demersal fish Myctophidae Jumbo squid Euphausids Pelagic red crab Macrobenthic invertebrates Shrimps Zooplankton Meiobenthos Phytoplankton Detritus

0.01 (5) 0.03 (11, 15)a 0.02 (5) (21) 0.19 (16, 19) 1.11 (3) 5.74 (10) 1.79 (14) 0.86 (14) 0.57 (12) 1.1a 2.7 (1) 0.83 (14) 0.59 (14, 18) 12 (5) 2.11 (14)

P/B per year

Q/B per year

0.38 (10) 0.03 (17) 0.08 (10) 0.47 (5) 1.26 (16) 0.88 (14) 4.5 (14) 0.96 (9) 1.59 (14) 3.25 (8, 12)d 7 (7) 1.2 (6) 3.48 (9) 2.29 (18) 25.68 (14) 11.28 (9) 95.95 (5)

73.8 (10) 5.27 (11)b 20.3 (10) 7.63 (5) 9.75 (4, 20)c 5.2 (14) 15.7 (14) 3.78 (9) 7.26 (14) 13.8 (2)e 24.9e 17.4 (14) 12.7 (9) 26.2 (10) 86.3 (14) 39.5 (9)

EE

0.74 0.7 0.96 0.94 0.87 0.8

0.9 0.9 0.9

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 corresponding to numbers: (1) Mathews et al. (1975); (2) Klett (1981); (3) Pérez-Mellado and Findley (1985); (4) Ehrhardt (1991); (5) Martínez-Tortolero (1994); (6) ˜ (1999); (11) Clarke and Paliza (2000); Balart (1996); (7) Gómez et al. (1996); (8) Klett (1996); (9) Godínez-Domínguez et al. (1999); (10) Pérez-Espana (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 b c d e

Mean weight × number of organisms (standardized to m2 ). Consumption/biomass. ln(Q/B) = −0.178 − 0.202 ln W∞ + 0.612 ln T + 0.516 ln A + 1.26F. P = B/42e(5.21 − 0.752 ln t) . Q = (R + P)/(EA).

country and probably the most dramatic case of a widely oscillating fishery in the Gulf of California (Lluch-Cota et al., 2007). The causes of this variability are unknown, but hypotheses range from hydrographic and biological processes (migratory responses of mainly small pelagic populations to prey availability, reproductive success and recruitment: Klett, 1981; Ehrhardt et al., 1982, 1986). However there is strong evidence that ENSO event is the strongest interannual signal influencing the system and also jumbo squid (Robles and Marinone, 1987; Marinone, 1988; Lavín et al., 2003; Bazzino et al., 2007; Herrera-Cervantes et al., 2007; Lluch-Cota et al., 2007). Due to its abundance, feeding behavior and its importance as a fishery resource, jumbo squid is an important species in the food web of the pelagic ecosystem in the Gulf of California. Changes in its abundance may influence population size and distribution of its predators and the energy flow patterns and function of the pelagic ecosystem (Cury et al., 2000; Menge, 2000; Achá and Fontúrbel, 2003). Therefore the objective of this study was to determine the importance and function of the jumbo squid in the tropic flows of the pelagic ecosystem in the central portion of the Gulf of California, through the implementation of two trophic models of biomass flows (Christensen and Pauly, 1993). One model was build for the year 1980 when squid fishery was incipient and the other for the year 2002 when the fishery was well established. In this way we could compare the ecosystem taking into account the different abundance of jumbo squid as a main factor.

2.

Materials and methods

2.1.

Description of Ecopath trophic flow model

The balance of biomass flows in the Ecopath type models is described 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

i

EEi −

n Q  

Bj

j=1

B

j

DCji − Yi − Ei − BAi = 0

(1)

where B = biomass (i prey, j predator; functional group given), P/B = production/biomass, proportion which equals to the instant total rate of mortality (Z), in a condition of balance (Allen, 1971), EEi = ecotrophic efficiency which represents the fraction of production either consumed or fished from the system, (Q/B)j = biomass/group consumption j, DCji = group fraction i in the predators diet j. Yi is the total fishery catch rate of (i). Ei the net migration rate. BAi is the biomass accumulation rate for (i). Eq. (1) represents the balance in the group’s biomass i in the ecosystem. Every group are represented by a similar equation, these simultaneous linear equations are solved by using matrix algebra (Walter, 1979). The groups in the model are represented by these equations and trophic interactions between groups are described by a diet matrix that quantitatively describes the fractions that each group has in each others groups diet.

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Construction of the pelagic ecosystem model in the central portion of the Gulf of California for 1980 and 2002. A total of 18 representative functional groups were selected each of them integrated by one or several species with a similar trophic role within the ecosystem. Out of the 18 functional groups (Table 1), one is a primary producer, one stands for detritus, one for zooplankton, six invertebrates, five for bony fish, one for cartilaginous fish, two for marine mammals and one for sea birds. Sperm whale (Physeter macrocephalus), jumbo squid (D. gigas) and the pelagic red crab (Pleuroncodes planipes) were treated individually as they are of particular interest for this study. For each functional group, input parameters (biomass, mortality, production/biomass P/B, ecotrophic efficiency EE, diet composition and food intake, and fishery data) were taken from the available literature (see Table 1) and standardized to units of ton km−2 year−1 . For the 1980 simulation modifications were made only in diet and biomass of jumbo squid group. Due to the absence of verified data of other group parameters two assumptions were made: (1) The P/B, Q/B and EE values from all the functional groups are the same for both years 1980 and 2002. (2) The nutritional regimen for the functional groups was the same for both models as there is no reliable data of diet for the 1980 groups, with the exception of jumbo squid.

2.2.

Biomass

2

B = average weight(organism number × area km )

(2)

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

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 calculated by using Eq. (3) (Kavanagh, 2002): P=

B 42

e(5.21−0.752

ln t)

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 the growth curve of von Bertalanfy, T = average temperature of the habitat in ◦ C, A = aspect ratio of the fin = h2 /s (h is the height and s the surface area of the fin), F = type of nutrition (0 for carnivorous, 1 for herbivorous and 0.5 for omnivorous) The value of Q/B for the sperm whale group was obtained by dividing the consumption reported by Clarke and Paliza (2000) by the sperm whale biomass in the area; for the squid data was taken from Klett (1981) and Markaida-Aburto (2001) using the 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 of 80% for animals.

Ecotrophic efficiency

One of the basic assumptions of steady state models is that the terms of the equations balance out. The program calculates the ecotrophic efficiency. But for nine groups (pelagic sharks, large pelagic fish, medium pelagic fish, minor pelagic fish, demersal fish, myctophids, macrobenthic invertebrates, zooplankton and phytoplankton) the values reported by 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 the Anuario estadistico de pesca (2002). For squid they were taken from landing data provided by the fisheries office in Santa Rosalia B.C.S. and Guaymas in Sonora for 2002. The capture values used in the 1980 model, were taken from Casas-Valdez and Ponce-Díaz (1996) for pelagic sharks, large and medium pelagic fish; Ehrhardt et al. (1980) for demersal fish, Ehrhardt et al. (1986) for jumbo squid, De Anda et al. (1994) for small pelagic fish and from Margallon (1987) and López et al. (2000) for shrimp, all values are reported in Table 2.

(3)

2.7.

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

2.4.

ln

2.5.

Biomass values were compiled from information reported in different studies form the area (Table 1). Jumbo squid biomass in 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 the 2002 model were calculated by using Eq. (2), considering abundance reported by Clarke and Paliza (2000) and Jaquet et al. (2003) for the sperm whale, and by Lavaniegos et al. (1989) for euphausids.

2.3.

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

Q/B relation

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

Diet matrix

Diet composition of the different functional groups in 2002 was estimated based on the reported studies of stomach content analysis. The citations are listed in Table 3 where also the proportion of each prey group in the diet is shown. For the simulation of the system in 1980 the diet composition for the jumbo squid was taken from Ehrhardt et al. (1986) (Table 3).

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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 1980

Pelagic shark Large pelagic fish Medium pelagic fish Small pelagic fish Demersal fish Jumbo squid Shrimps

2.8.

0.02

Mayor ships 2002

0.28

The models were balanced by adjusting the input parameters so that EE values were