Ecosystems (2013) 16: 416–433
DOI: 10.1007/s10021-012-9618-z
The Ecological Role of the Vaquita,
Phocoena sinus, in the Ecosystem of
the Northern Gulf of California
Marjorie Riofrı́o-Lazo,1,2* Francisco Arreguı́n-Sánchez,2
Manuel Zetina-Rejón,2 and Fabián Escobar-Toledo2
1
Galapagos Science Center, Universidad San Francisco de Quito (USFQ) and The University of North Carolina at Chapel Hill (UNC),
Ave. Alsacio Northia, Pto. Baquerizo Moreno, San Cristóbal Island, Galápagos, Ecuador; 2Centro Interdisciplinario de Ciencias
Marinas, Instituto Politécnico Nacional, P.O. Box 592, 23060 La Paz, BCS, Mexico
ABSTRACT
From an ecosystem management perspective, anal-
ysis of the functional roles of species is a challenge. It
is valuable to determine which species are irre-
placeable within a given community based on their
contribution to the system’s organization. This study
relates the emergent functional and structural indi-
ces of biological groups estimated from a trophic
model of the Northern Gulf of California to identify
the roles of these groups in the ecosystem context,
with a particular focus on the role of the vaquita, an
endemic porpoise in critically endangered status. The
simulation of removing each group allowed the
analysis of the removal’s functional effect on the
ecosystem’s global attributes and organization (based
on Ulanowicz’s ascendency concept). Groups from
lower trophic levels (TL) were more related to com-
plexity indicators, suggesting their contribution to
the organization and structure of energy flows in the
food web. Groups from intermediate TL had higher
values of structural indexes, indicating their function
Received 11 January 2012; accepted 5 October 2012;
published online 6 December 2012
Authors Contributions: MR designed methods, analyzed data and
wrote the paper. FA conceived and designed study, analyzed data and
reviewed drafts. MZ designed study, analyzed data and reviewed drafts.
FE analyzed data. All the authors participated in the interpretation and
discussion of the results.
*Corresponding author; e-mail: marjorieriofrio@gmail.com
416
 2012 Springer Science+Business Media New York
in the control of flows throughout the network. The
vaquita along with other marine mammals, aquatic
birds, and some species of fish with a high TL con-
tribute in a similar way to the order (for example,
ascendency/capacity-of-development ratio) of the
system, showing a relatively high value of ascen-
dency (contribution of the group to the organization
inherent to the ecosystem) and the change in eco-
system ascendency when they were removed. The
vaquita, like marine and coastal birds, plays a small
role in the ecosystem. But like them, it does con-
tribute substantially to ecosystem organization. This
study thus provides information potentially useful
for management in understanding the species’ role
and in reducing uncertainty in decision-making.
Key words: vaquita; Northern Gulf of California;
role of groups; emergent network indices; trophic
ecosystem model; ecosystem order; ecosystem
functioning; energy flows.
INTRODUCTION
The Gulf of California hosts diverse ecosystems and
important fisheries that support industry and pro-
vide a livelihood to coastal settlements (Lluch-Cota
and others 2007). Physical and biological charac-
teristics vary significantly along the gulf (Lercari
and others 2007). The Northern Gulf of California
(NGC), an area of 36,000 km2, is partially isolated
 Role of the Vaquita in the Northern Gulf of California
from the rest of the Gulf by the Angel de la Guarda
and Tiburón islands to the south (Figure 1). The
northernmost portion (regionally called the Upper
Gulf of California) consists of the delta and mouth
of the Colorado River, and it is relatively shallow
(2–30 m) in comparison with the deeper (200–
400 m) southern region (Lercari and Arreguı́n-
Sánchez 2008).
Long-term studies have documented dramatic
changes in sea surface water temperatures and
floral/faunal community structure from winter to
summer in the NGC, but it is essentially a tropical
environment (Lluch-Cota and others 2007). The
Colorado River supplies freshwater, silt, and
nutrients to this region (Glen and others 1996). The
reduction in the river’s flow due to dams and water
extraction since the 1930s has completely trans-
formed the region from an estuarine system into an
anti-estuary (Lavı́n and Sánchez 1999; Brusca and
others 2004), thereby reducing the critical habitats
for many species (Aragón-Noriega and Calderón-
Aguilera 2000). Despite this change, the Upper Gulf
is still considered one of the most productive
regions of the Gulf of California (Alvarez-Borrego
2010), and it is a natural refuge for thousands of
species, including commercial, endemic, and some
endangered species (Lluch-Cota and others 2007).
There are two famous species endemic to the NGC,
both of which are classified as critically endangered.
One of these species, the totoaba, Totoaba macdonaldi,
is among the largest members of the Sciaenidae and
experienced heavy fishing exploitation several dec-
ades ago (Contreras-Balderas and Almada-Villela
417
1996). The other, the vaquita, Phocoena sinus, is a
small porpoise with a mean estimated population
size of approximately 245 individuals (Gerrodette
and others 2011) and is one of the world’s most
emblematic marine mammals. The distribution of
this marine mammal is confined to a small area
between Rocas Consag and San Felipe Bay (Rojas-
Bracho and others 2006), where it has been observed
in shallow waters (generally from 10 to 50 m) at
distances of 11–25 km from the coast (Silber and
others 1994; Gallo-Reynoso 1998). It is observed in
groups of no more than seven individuals (Silber and
others 1994), and it feeds mainly on a variety of small
demersal fish, squid, and crustaceans (Pérez-Cortés
and others 1996).
Ecological competition between fisheries and
vaquitas has not yet been suggested in the litera-
ture, although several prey species of the vaquita’s
diet have been reported as by-catch in trawl nets
(Nava-Romo 1994; Pérez-Cortés and others 1996).
Trawling alters benthic-demersal communities by
reducing structure and biodiversity (Nava-Romo
1994). The intensity of trawling disturbances when
combined with the extremely restricted distribu-
tion of vaquitas in the Upper Gulf could have
important effects on the foraging, reproductive and
aggregating behaviors of these animals (Jaramillo-
Legorreta and others 1999; Rojas-Bracho and oth-
ers 2002).
There are other less well-characterized and
longer term risk factors to vaquita populations,
such as pollution by organochlorides, habitat
alteration caused by reduced flow from the Colorado
Figure 1. Map of the NGC
showing the marine
protected areas. The
Upper Gulf of California
and Colorado River
Biosphere reserve: core
zone (1), buffer zone (2),
and the Vaquita
Conservation Refuge
(striped polygon).
418 M. Riofrı́o-Lazo and others
River, and the deleterious effects of inbreeding
(Rojas-Bracho and others 2006). However, inci-
dental entanglement in gillnets used by a portion of
the artisanal fishing fleet to catch sharks and other
fish is clearly the major threat to vaquita survival
(D’Agrosa and others 2000) and requires immedi-
ate attention.
In an effort to protect vaquita, the Upper Gulf of
California and Colorado River Delta Biosphere
Reserve was established in 1993, but it has fallen
far short of its potential for vaquita conservation
(Rojas-Bracho and others 2006). Therefore, in
2005, a Vaquita Conservation Refuge was estab-
lished that extends beyond the previous reserve
boundary (Lercari and others 2007). Despite the
conservation actions, the decline in abundance of
the vaquita has been estimated at 7.6% per year
between 1997 and 2008, and a total decline of 57%
over the 11-year period (Gerrodette and others
2011), showing the species in clear danger of
extinction.
Although there is a general consensus regarding
the importance of the conservation of this ecosys-
tem and many conservation efforts have been
focused on vaquita, the role of this species has not
yet been analyzed in the context of the ecosystem
health and functioning. A proxy method for
determining the overall health of the ecosystem is
food web modeling. The Ecopath approach allows
for the identification of the trophic role of endan-
gered species, top predators, and fleets (fishing
pressure and landings) on ecosystem components
(Lercari and others 2007). Models can provide a
scientifically based representation of ecosystem
structure and functioning from which to derive
indicators and reference points and to simulate the
effects of management actions (Brodziak and Link
2002). Several trophic models of ecosystem func-
tion in selected environments of the Gulf of Cali-
fornia have already been used to explore
management scenarios and potential fishing im-
pacts (Lluch-Cota and others 2006). In the north-
ern gulf, evaluated management scenarios suggest
that conservation and fishing could be compatible
under an appropriate management scheme, which,
in terms of the simulations, implies proper control
of fishing (Lercari and others 2007).
In setting optimal conservation priorities for
ecosystem management it is important to identify
the ecological contributions and roles of species in
the ecosystem. Thus, keystone species, which
affect community structure disproportionately to
their biomass (Power and others 1996) and
strongly influence the ecosystem dynamics (Piraino
and others 2002), deserve particular attention in
conservation practice (Jordan 2009). However,
attempts should also be made to protect and
manage those species subjectively considered to
be important or vulnerable. Also important are
those species that transfer energy to higher tro-
phic levels (TL) and those which are well con-
nected with species of high economic or
conservation value.
Ecosystem network analysis indices, such as the
Finn cycling index (FCI), ascendency, redundancy
or internal flow overhead, systems entropy (H),
total systems throughput (TST), and average
mutual information (AMI) (Vasconcellos and others
1997; Mageau and others 1998; Ulanowicz 2001;
Heymans and others 2002; Heymans and others
2007), have previously been used as indicators of
ecosystem stability and stress, and these could
provide valuable insights into the ecological roles of
species. In this study, we use several network
analysis indices estimated from a previously
published mass-balanced Ecopath trophic model
(version 5.1) of the NGC (Lercari and Arreguı́n-
Sánchez 2008) and some ecological attributes of the
functional groups to analyze the ecological roles of
the groups in the context of ecosystem functioning.
We discuss which groups are related to the pres-
ervation of ecosystem order and structure, and
highlight the ecological role and the importance of
the vaquita in the ecosystem.
METHODS
Data
We used data from a previously published mass-
balanced model of the NGC ecosystem (Lercari and
Arreguı́n-Sánchez 2008). It represents the ecosys-
tem state for the decade 1990–2000. The model
considered 34 functional groups: four groups of
marine mammals, two groups of birds, 18 fish, nine
invertebrates, one zooplankton, one phytoplank-
ton, one macroalgae, and one detritus. These
groups represent the most abundant species in the
NGC. In addition, T. macdonaldi, P. sinus, Zalophus
californianus and the shrimp species Farfantepenaeus
californiensis and Litopenaeus stylirostris were
included as single species groups to explicitly rep-
resent species with noteworthy economic, social, or
ecological values. For further details regarding the
model, see Lercari and Arreguı́n-Sánchez (2008).
To explore the role of each group, we constructed
a data matrix based on indices related to the con-
tribution of each group to ecosystem structure and
functioning emphasizing relationships among
groups instead indices.
 Role of the Vaquita in the Northern Gulf of California
Structural Indices
The indices related to ecosystem structure were
obtained from the Ecopath model results and include
the following measures for each group: biomass (B, t
km2), respiration (R, t km2 y-1), production/biomass
(P/B, y-1), consumption/biomass (Q/B, y-1), respi-
ration/biomass (R/B, y-1), trophic level (TL, dimen-
sionless), production/consumption (P/Q, y-1),
production/respiration (P/R, dimensionless), omni-
vory index (OI, dimensionless), and respiration/
assimilation (R/As, dimensionless). In addition, two
attributes of the groups, the Degree index
(D, dimensionless) and the Keystone index (Ki,
dimensionless), were estimated using data from the
predator–prey consumption matrix obtained from
the Ecopath model (Table 1). D, the number of
connections or edges the node has to other nodes,
was estimated as by Jordan and others (2006):
Di = Din,i + Dout,i; where the degree of a node i (Di) is
the sum of its prey (in-degree: number of incoming
edges, Din,i) and predators (out-degree: number of
outgoing edges, Dout,i). This index characterizes only
the number of its connected (neighbor) points,
whereas the Ki index also gives information on how
these neighbors are connected to other neighbors
and is calculated by Jordan and others (2006) as:
X
n
1 X Ti;j 
Ki ¼ Kbu;i þ Ktd;i ¼ Kdir;i þ Kindir;i ¼ ð1 þ Kbc Þ
dc
c¼1
X
m
1
þ ð1 þ Kte Þ
f
e¼1 e
where n is the number of predators eating species i,
dc is the number of prey of its cth predator, and Kbc
represents the bottom-up keystone index of the cth
predator. Symmetrically, m is the number of prey
eaten by species i, fe is the number of predators of
its eth prey and Kte represents the top-down key-
stone index ofPthe eth prey. For node i, the first
sum, that is, 1/dc (1 +/Kbc) quantifies the bot-
tom-up
P effect (Kbu,i ), whereas the second sum, that
is, 1/fe (1 +/Kte) quantifies the top-down effect
(Ktd,i). After rearranging P equation,Pterms including
Kbc and Kte (that is, Kbc/dc + Kte/fe) refer to
indirect effects for node i (Kindir,i),PwhereasP terms
not containing Kbc and Kte (that is, 1/dc + 1/fe)
refer to direct ones (Kdir,i). Both Kbu,i + Ktd,i and
Kdir,i + Kindir,i equals Ki. It emphasizes vertical over
horizontal interactions (for example, trophic cas-
cades as opposed to apparent competition) but
characterizes positional importance by separating
bottom-up from top-down effects in food webs
(Jordan and others 2006).
419
Functional Indices
The indices used in the analysis with regards to
ecosystem functioning were the AMI, the effective
number of roles (Ro), the ascendency (A), the
overhead (U), and the development capacity (C).
These indices were estimated using data from the
predator to prey consumption matrix obtained
from the Ecopath model. AMI and Ro were mea-
sured for each functional group of the system,
whereas A, U, and C were calculated by removal
simulations of each one of the groups on those
global attributes of the ecosystem related to
Ulanowicz’s ascendency concept. That is, by
extraction of a group i, it ceases to contribute to the
system, thereby allowing its relative contribution to
the ascendency, overhead, and/or development
capacity of the system to be determined.
The AMI index, expressed in bits, measures the
organization of the exchanges among groups
(Ulanowicz 1986). An increase in AMI implies that
the system is becoming more constrained and is
channeling flows along more specific pathways
(Ulanowicz and Abarca-Arenas 1997), representing
a more developed ecosystem. Following Ulanowicz
(1986) and based on information theory, the AMI
was calculated for each functional group as

Tij T::

AMI ¼ log
i;j
T:: Ti: T:j
where T.. is the total sum of all flows, also known as
the total system throughput (Ulanowicz 2002). Ti.
and T.j are the output and input throughputs of a
node, respectively; Ti. represents the total flow of
biomass that leaves i during the unit time interval,
whereas T.j gauges the total flow of biomass
entering j during that same duration (Ulanowicz
and others 2009).
The effective number of roles (Ro) is a dimension-
less index that measures the degree to which the
system has become differentiated into distinct func-
tions and has an analog in information theory:
logRo = AMI (Zorach and Ulanowicz 2002). Thus, we
estimate the role of each functional group (Roi) as eAMI.
Ascendency is one of the attributes of the eco-
system that quantifies the level of system activity
and the degree of its organization (Ulanowicz
1980). The ascendency of a system should increase
as the system matures through a series of devel-
opmental stages, and it is estimated by Ulanowicz
and Norden (1990) as
X  
Tij T::
A¼ Tij log
i;j
Ti: T:j
Table 1. Predator–Prey Matrix Representing Diet Composition for Groups in the NGC Ecosystem Model
420

Prey Predator

1 2 3 4 5 6 7 8 9 10 11 12 13

1. Sharks 0.022 0.010 0.002 0.092

2. Z. californianus
3. T. macdonaldi
(Adults)
4. Marine birds
5. Odontoceti 0.004
6. P. sinus
7. T. macdonaldi 0.002 0.005
(Juveniles)
M. Riofrı́o-Lazo and others

8. Merluccidae 0.011 0.014

9. Mysticeti
10. Coastal birds
11. Sciaenidae 0.267 0.023 0.006 0.002 0.101 0.005 0.037 0.034
12. Rhinobatidae 0.011 0.023 0.003 0.002
13. Serranidae 0.004 0.000 0.004
14. Rays 0.011 0.023 0.001 0.101 0.041 0.004
15. Other fish 0.888 0.201 0.003 0.007 0.956 0.007 0.014 0.077 0.620 0.062 0.012
16. Haemulidae 0.011 0.005 0.003 0.005 0.001 0.012
17. S. penicillata 0.002 0.001 0.004 0.003 0.002
18. Small pelagics 0.486 0.115 0.019 0.011 0.947 0.008 0.055 0.042 0.065 0.024
19. F. californiensis 0.006 0.001 0.003
(Juveniles)
20. L. stylirostris 0.001 0.003
(Juveniles)
21. Cephalopoda 0.043 0.035 0.003 0.003 1.480 0.004 0.003 0.116
22. Flat fish 0.011 0.002 0.003
23. Myctophidae 0.389 0.060 0.901 0.006 0.087 0.027 0.101
24. Mojarras 0.011 0.049 0.003 0.046 0.004 0.012 0.002 0.001
25. Callinectes sp 0.002 0.002 0.019 0.001 0.012 0.039 0.001
26. Polychaeta 0.002 0.019 0.018 0.017 0.002 0.199 0.068 0.004
27. Stomatopoda 0.001 0.001 0.006 0.010 0.003
28. L. stylirostris 0.003 0.005 0.004 0.027 0.003 0.001 0.001 0.498 0.005 0.002
(Adults)
29. Benthic 0.028 0.009 0.054 0.001 0.778 0.084 0.018
invertebrates
30. F. californiensis 0.005 0.002 0.001 0.001 0.125 0.001
(Adults)
31. Zooplankton 0.026 0.091 0.001
Table 1. continued
Prey Predator
1 2 3 4 5 6 7 8 9 10 11 12 13

32. Phytoplankton
33. Macrophites 0.007
34. Detritus 0.400 0.079 0.012

Prey Predator
14 15 16 17 18 19 20 21 22 23 24 25

1. Sharks
2. Z. californianus
3. T. macdonaldi
(Adults)
4. Marine birds
5. Odontoceti
6. P. sinus
7. T. macdonaldi
(Juveniles)
8. Merluccidae 0.001
9. Mysticeti
10. Coastal birds
11. Sciaenidae 0.002
12. Rhinobatidae 0.002 0.001
13. Serranidae
14. Rays 0.006 0.005 0.029
15. Other fish 0.148 0.319 0.197 0.144
16. Haemulidae 0.015
17. S. penicillata 0.002 0.002 0.001 0.002 0.002 0.028
18. Small pelagics 3.104
19. F. californiensis 0.015 0.006 0.017 0.014 0.024 0.009 0.010 0.051
(Juveniles)
20. L. stylirostris 0.015 0.006 0.017 0.014 0.024 0.009 0.010 0.101
(Juveniles)
21. Cephalopoda 0.738 0.002 3.045 0.002 0.548
22. Flat fish 0.002 0.002 0.002
23. Myctophidae 0.014
24. Mojarras 0.084 0.002
25. Callinectes sp 0.002 0.039
Role of the Vaquita in the Northern Gulf of California

26. Polychaeta 0.464 1.493 0.044 0.724 0.541 0.478

27. Stomatopoda 0.002 0.015 0.020 0.051
421
Table 1. continued
422

Prey Predator
14 15 16 17 18 19 20 21 22 23 24 25

28. L. stylirostris 0.021 0.016 0.020 0.012 0.001 0.004 0.051

(Adults)
29. Benthic 0.892 1.460 0.182 0.064 0.242 0.271 1.011
invertebrates
30. F. californiensis 0.011 0.020 0.001 0.004 0.005
(Adults)
31. Zooplankton 3.524 0.197 0.022 12.79 1.069 3.080 13.32 0.002 4.903 0.242
32. Phytoplankton 1.896 0.160 0.009 3.642 0.306 0.880 9.787 3.269 0.242
33. Macrophites 0.068 2.668 0.004 0.076 0.220 0.024 0.368 0.450
34. Detritus 0.492 1.393 0.196 0.040 0.076 0.220 1.006 1.208 0.548 0.737 2.871
M. Riofrı́o-Lazo and others

Prey Predator
26 27 28 29 30 31 32 33 34 Flow to detritus Respiration Exportation

1. Sharks 0.485 1.533 0.027

2. Z. californianus 0.108 0.394 0.000
3. T. macdonaldi 0.009 0.029 0.002
(Adults)
4. Marine birds 0.007 0.028 0.000
5. Odontoceti 0.957 3.641 0.000
6. P. sinus 0.010 0.035 0.000
7. T. macdonaldi 0.046 0.147 0.001
(Juveniles)
8. Merluccidae 0.082 0.151 0.013
9. Mysticeti 0.070 0.192 0.000
10. Coastal birds 0.001 0.005 0.000
11. Sciaenidae 0.840 1.697 0.038
12. Rhinobatidae 0.007 0.114 0.210 0.017
13. Serranidae 0.016 0.041 0.005
14. Rays 0.503 1.304 0.083
15. Other fish 3.561 9.308 0.252
16. Haemulidae 0.232 0.600 0.112
17. S. penicillata 0.053 0.082 0.000
18. Small pelagics 3.551 8.026 0.012
19. F. californiensis 0.001 0.000 1.370 0.000
(Juveniles)
20. L. stylirostris 0.028 0.000 4.170 0.000
(Juveniles)
21. Cephalopoda 7.445 13.72 0.000
Table 1. continued
Prey Predator
26 27 28 29 30 31 32 33 34 Flow to detritus Respiration Exportation

22. Flat fish 0.526 1.809 0.088

23. Myctophidae 1.943 5.727 0.034
24. Mojarras 0.575 1.049 0.128
25. Callinectes sp 2.647 2.853 0.000
26. Polychaeta 13.13 0.067 0.218 20.89 0.165 29.41 68.97 0.000
27. Stomatopoda 0.001 0.153 0.294 0.017
28. L. stylirostris 0.003 0.000 2.868 0.281
(Adults)
29. Benthic 26.15 0.054 0.692 12.92 0.164 89.81 107.36 0.178
invertebrates
30. F. californiensis 0.003 0.000 1.272 0.140
(Adults)
31. Zooplankton 6.573 0.006 0.329 42.89 0.137 406.53 636.75 900.18 0.000
32. Phytoplankton 6.573 0.022 0.329 58.15 0.112 1422.86 5271.76 0.000 0.000
33. Macrophites 6.162 0.004 0.096 30.77 0.023 55.66 0.000 0.003
34. Detritus 78.33 0.376 2.161 76.81 0.991 203.26 0.000 0.000 0.000

Data were taken from Lercari and Arreguı́n- Sánchez (2008). Last three columns are data required, in addition to prey-predator matrix, to compute several indices used.
Role of the Vaquita in the Northern Gulf of California
423
424 M. Riofrı́o-Lazo and others
where the variables are the same as used for the
estimation of AMI. The complement to the ascen-
dency is the overhead (/), which measures the
disorder, incoherent, and dissipative information
that a system retains and is calculated as
! aggregated with a strong effect on ascendency
X Tij2
/¼ Tij log
i;j
Ti: T:j
In addition, Ulanowicz’s theory postulates that a
system’s ascendency and overhead sum to yield its
overall development capacity (C = A + /). The
ascendency and the capacity will decrease if the
system is affected by disturbance or pollution stress
(Baird and Ulanowicz 1993). Ascendency, over-
head, and development capacity are expressed in
flowbits or as the product of flows and bits
(t km2 y-1 bits).
For purposes of comparison, A is commonly
expressed as proportional to C; in this manner, the
relative ascendency ratio (A/C) can represent the
degree of growth, organization, and development
of a system (Ulanowicz and Mann 1981). Based on
this index, the following ratios were derived to
measure the functional role of each group: the
ðA=CÞexti is the relative change in the ascendency
ratio calculated when group i is extracted from the
system; the Aexti =A0 is the relative change in
ascendency when group i is extracted from the
system, with respect to the original ascendency
(Ao = 15043.111); and the ðA=CÞexti =ðA=CÞ0 is the
proportional change due to ðA=CÞexti , with respect
to the original (A/C)o ratio, (A/C)o = 0.5182.
Data Analysis
The similarity between structural and functional
indices was identified using a non-metric multi-
dimensional scaling (MDS) test. The MDS was
performed using a Bray–Curtis similarity coefficient
matrix estimated from the log(x + 1) transformed
data matrix. This analysis represents all indices in
two-dimensional space such that the relative dis-
tances between all points are in the same rank
order. Indices that are closer are more similar than
those that are further apart (Clarke and Gorley
2006). In this way, we were able to discard
redundant indices and to select those indices that
were not similar to others (within each group in
the MDS analysis).
We performed a principal components analysis
(PCA) using only the indices selected from the
MDS analysis. The PCA allows us to summarize the
information about the structural and functional
indices of each group to identify which of them had
similar roles. Six functional groups (detritus, mac-
rophytes, phytoplankton, zooplankton, benthic
invertebrates, and polychaeta) were not included
in the PCA to avoid bias because they occupy either
basal or low TL, and usually, they are highly
estimations. Abarca-Arenas and Ulanowicz (2002)
have shown that highly aggregated groups could
significantly affect the values of the ascendency
index, especially at low TL. All values were stan-
dardized before running the PCA. Only the prin-
cipal components with eigenvalues higher than
one were retained and the contribution of the
functional groups to the explained variance of PC
was analyzed. Finally, we used the Spearman’s
rank correlation coefficient (rs) to analyze the
relationship between selected indices. This test was
used because the indices did not follow a normal
distribution (Shapiro–Wilk: P < 0.05). Statistical
analyses were performed using Primer version 6.0
and Statistica version 8. Statistical significance was
assumed at P < 0.05.
RESULTS
The values of the ecological indices estimated for all
functional groups are shown in Table 2. MDS
analysis identified the relative rankings of the
similarities among the variables with a stress level
of 0.02 (Figure 2). According to Clarke (1993), a
stress level less than 0.05 indicates an accurate
representation with no prospect of misinterpreta-
tion. MDS test revealed two different groups of
indices that were not at all similar. The first, formed
by Ascendency (A), Development Capacity (C), and
Overhead (O), have 80% similarity; the second
group, with different sub-groups was also formed
according to the per cent of similarity between
them. The highest percent similarity (80%) was
found between Q/B and R/B, TL and K, P/R and OI,
and among R/As, AMI, Roi, Aexti =A0 and
ðA=CÞexti =ðA=CÞ0 . Accordingly, the following indices
were selected for the PCA: A, R/B, TL, OI, Roi, B,
P/B, P/Q, R, D, and ðA=CÞexti . Those variables were
selected because they are representative of groups
with 80% of similarity.
The PCA constructed using the selected indices
and functional groups showed six different group-
ings with similar roles (Figure 3): (1) juveniles and
adults of both species of shrimps (Farfantepenaeus
californiensis and Litopenaeus stylirostris) and the
crab, Callinectes spp.; (2) cephalopoda; (3) small
pelagics and myctophidae; (4) other fish; (5) sharks
and odontoceti; and (6) other groups including the
vaquita.
 Role of the Vaquita in the Northern Gulf of California 425

Table 2. Functional Groups, Input and Estimated Values of a Selection of Parameters of the NGC Ecosystem
Model
Functional group TL B P/B Q/B P/Q OI R R/As P/R R/B

1. Sharks 4.030 0.723 0.280 3.000 0.093 0.050 1.533 0.883 0.132 2.120
2. Z. californianus 3.970 0.014 0.544 35.470 0.015 0.054 0.394 0.981 0.020 27.832
3. T. macdonaldi (Adults) 3.960 0.008 0.414 5.000 0.083 0.073 0.029 0.897 0.115 3.586
4. Marine birds 3.950 0.000 0.500 89.000 0.006 0.101 0.028 0.993 0.007 70.700
5. Odontoceti 3.930 0.174 0.236 26.449 0.009 0.046 3.641 0.989 0.011 20.923
6. Phocoena sinus 3.920 0.002 0.600 30.000 0.020 0.085 0.035 0.975 0.026 23.400
7. T. macdonaldi (Juveniles) 3.820 0.020 0.700 10.272 0.068 0.140 0.147 0.915 0.093 7.518
8. Merluccidae 3.790 0.147 0.450 1.850 0.243 0.062 0.151 0.696 0.437 1.030
9. Mysticeti 3.550 0.090 0.200 2.920 0.068 0.087 0.192 0.914 0.094 2.136
10. Coastal birds 3.450 0.000 0.250 45.000 0.006 0.009 0.005 0.993 0.007 35.750
11. Sciaenidae 3.440 0.252 2.950 12.100 0.244 0.380 1.697 0.695 0.438 6.730
12. Rhinobatidae 3.320 0.150 0.680 2.600 0.262 0.508 0.210 0.673 0.486 1.400
13. Serranidae 3.260 0.020 0.790 3.600 0.219 0.640 0.041 0.726 0.378 2.090
14. Rays 3.100 0.414 0.930 5.100 0.182 0.461 1.304 0.772 0.295 3.150
15. Other fish 3.020 2.109 1.950 7.954 0.245 0.634 9.308 0.694 0.442 4.413
16. Haemulidae 3.010 0.069 2.850 14.400 0.198 0.637 0.600 0.753 0.329 8.670
17. S. penicillata 3.000 0.022 3.000 8.500 0.353 0.414 0.082 0.559 0.789 3.800
18. Small pelagics 2.970 1.560 3.300 10.556 0.313 0.271 8.026 0.609 0.641 5.145
19. F. californiensis (Juveniles) 2.880 0.038 8.500 40.189 0.211 0.328 1.370 1.121 0.236 36.045
20. L. stylirostris (Juveniles) 2.880 0.119 9.000 37.106 0.243 0.328 4.170 1.185 0.256 35.167
21. Cephalopoda 2.820 2.328 3.450 11.680 0.295 0.470 13.720 0.631 0.585 5.894
22. Flat fish 2.770 0.229 0.650 10.700 0.061 0.632 1.809 0.924 0.082 7.910
23. Myctophidae 2.770 1.170 1.456 7.937 0.183 0.433 5.727 0.771 0.298 4.894
24. Mojarras 2.640 0.317 1.650 6.200 0.266 0.532 1.049 0.667 0.498 3.310
25. Callinectes sp 2.530 0.619 2.650 9.072 0.292 0.503 2.853 0.635 0.575 4.608
Polychaeta 2.470 5.071 8.000 27.000 0.296 0.446 68.967 0.630 0.588 13.600
26. Stomatopoda 2.460 0.066 2.500 8.700 0.287 0.520 0.294 0.641 0.561 4.460
27. L. stylirostris (Adults) 2.450 0.200 5.400 19.121 0.282 0.423 2.868 0.937 0.377 14.339
Benthic invertebrates 2.420 2.886 30.000 84.000 0.357 0.392 107.359 0.554 0.806 37.200
28. F. californiensis (Adults) 2.410 0.080 5.400 19.900 0.271 0.403 1.272 0.999 0.340 15.903
Zooplankton 2.250 29.038 25.000 70.000 0.357 0.250 900.178 0.554 0.806 31.000
Phytoplankton 1.000 113.000 60.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
Macrophites 1.000 1.610 60.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
Detritus 1.000 88.520 0.000 0.000 0.000 0.191 0.000 0.000 0.000 0.000

Functional group D K AMI Roi A O C ðA=CÞexti Aexti =A0 ðA=CÞexti =

ðA=CÞ0

1. Sharks 4.340 5.037 0.0004 1.0004 15193.49 13778.95 28972.44 0.5244 1.0100 1.0118
2. Z. californianus 1.004 2.490 0.0013 1.0013 15130.38 13881.69 29012.06 0.5215 1.0058 1.0063
3. T. macdonaldi (Adults) 0.078 1.389 0.0006 1.0006 15117.99 13906.46 29024.46 0.5209 1.0050 1.0050
4. Marine birds 0.070 1.821 0.0011 1.0011 15125.25 13899.33 29024.58 0.5211 1.0055 1.0055
5. Odontoceti 9.205 3.370 0.0012 1.0012 15214.09 13703.11 28917.19 0.5261 1.0114 1.0152
6. Phocoena sinus 0.091 2.602 0.0013 1.0013 15125.92 13898.34 29024.26 0.5211 1.0055 1.0055
7. T. macdonaldi (Juveniles) 0.402 1.799 0.0009 1.0009 15117.08 13902.05 29019.12 0.5209 1.0049 1.0051
8. Merluccidae 0.544 1.480 0.0014 1.0015 15065.83 13953.27 29019.10 0.5192 1.0015 1.0017
9. Mysticeti 0.523 1.158 0.0022 1.0022 15076.52 13943.53 29020.05 0.5195 1.0022 1.0024
10. Coastal birds 0.014 0.913 0.0011 1.0012 15137.95 13887.42 29025.37 0.5215 1.0063 1.0063
11. Sciaenidae 6.105 4.398 0.0002 1.0002 15109.65 13845.96 28955.61 0.5218 1.0044 1.0068
12. Rhinobatidae 0.780 2.361 0.0008 1.0008 15080.86 13936.06 29016.93 0.5197 1.0025 1.0028
13. Serranidae 0.139 2.388 -0.0014 0.9986 15129.37 13894.45 29023.82 0.5213 1.0057 1.0058
14. Rays 4.221 2.786 -0.0002 0.9998 15108.07 13875.31 28983.38 0.5213 1.0043 1.0058
15. Other fish 33.551 4.238 -0.0014 0.9986 15104.94 13631.52 28736.46 0.5256 1.0041 1.0142
16. Haemulidae 1.991 2.721 -0.0009 0.9991 15116.15 13886.92 29003.08 0.5212 1.0049 1.0056
17. S. penicillata 0.367 2.187 0.0008 1.0008 15071.53 13950.26 29021.80 0.5193 1.0019 1.0020
426 M. Riofrı́o-Lazo and others

Table 2. continued
Functional group D K AMI Roi A O C ðA=CÞexti Aexti =A0 ðA=CÞexti =
ðA=CÞ0

18. Small pelagics 32.932 1.849 0.0005 1.0005 14997.91 13799.18 28797.10 0.5208 0.9970 1.0049
19. F. californiensis (Juveniles) 3.054 2.534 0.0148 1.0149 15007.87 13990.67 28998.54 0.5175 0.9977 0.9986
20. L. stylirostris (Juveniles) 8.798 2.376 0.0134 1.0135 14997.31 13958.05 28955.37 0.5179 0.9970 0.9994
21. Cephalopoda 54.374 2.092 0.0096 1.0096 14846.72 13831.54 28678.26 0.5177 0.9869 0.9989
22. Flat fish 4.886 2.122 0.0005 1.0005 15117.81 13857.31 28975.12 0.5218 1.0050 1.0067
23. Myctophidae 18.578 2.142 -0.0010 0.9990 15069.24 13815.73 28884.97 0.5217 1.0017 1.0066
24. Mojarras 3.933 2.528 0.0010 1.0010 15073.65 13910.72 28984.38 0.5201 1.0020 1.0035
25. Callinectes sp 11.237 2.558 0.0117 1.0117 14898.49 14021.80 28920.29 0.5152 0.9904 0.9940
Polychaeta 273.841 3.705 0.0132 1.0133 14894.22 12328.67 27222.89 0.5471 0.9901 1.0557
26. Stomatopoda 1.146 2.717 0.0004 1.0004 15096.07 13916.98 29013.05 0.5203 1.0035 1.0040
27. L. stylirostris (Adults) 7.651 3.555 0.0101 1.0101 15017.71 13937.81 28955.52 0.5186 0.9983 1.0007
Benthic invertebrates 484.847 4.981 0.0126 1.0127 14514.32 11702.34 26216.66 0.5536 0.9648 1.0682
28. F. californiensis (Adults) 3.183 2.581 0.0107 1.0108 15023.33 13970.86 28994.19 0.5181 0.9987 0.9998
Zooplankton 4065.319 7.962 0.0185 1.0186 6556.20 10988.23 17544.43 0.3737 0.4358 0.7210
Phytoplankton 6780.001 11.217 0.0567 1.0583 10621.70 2772.82 13394.53 0.7930 0.7061 1.5301
Macrophites 96.601 6.184 0.0480 1.0492 14390.84 13785.62 28176.46 0.5107 0.9566 0.9855
Detritus 6478.528 17.817 0.1876 1.2063 -2505.73 13995.84 11490.11 -0.2181 -0.1666 -0.4208

TL, Trophic level; B, Biomass; P/B, Production/Biomass ratio; Q/B, Consumption/Biomass ratio; P/Q, Production/Consumption ratio; OI, Omnivory Index; R, Respiration;
R/As, Respiration/Assimilation ratio; P/R, Production/Respiration ratio; R/B, Respiration/Biomass; D, Degree index; K, Key species index; AMI, Average Mutual Information;
Roi, Role; A, Ascendency; O, Overhead; C, Development capacity. These last three calculated for the system without a specific functional group. Based on the relative ascendency
ratio index (A/C), three ratios were derived: ðA=CÞexti , the relative change in the ascendency ratio calculated when group i is extracted of the system; Aexti =A0 , the relative
change in ascendency when group i is extracted of the system respect to the original ascendency; ðA=CÞexti =ðA=CÞ0 , the proportional change due to ðA=CÞexti respect to the
original (A/C)o ratio Data were taken from Lercari and Arreguı́n-Sánchez (2008) and estimated from the predator–prey matrix Ecopath model of this ecosystem. The number at
the left of specific functional groups represents the identification key of the selected groups for the subsequent analyses.

Figure 2. Similarity
percentages among the
variables plotted in non-
metric multidimensional
scaling. The proximity of
one variable to the next
represents similarity, and
the circles represent the
two-dimensional
ordinations of the ranked
orders of similarity among
variables. Open and filled
gray circles show the 60
and 80% of similarity,
respectively. The data are
log(x + 1) transformed.
Resemblance: S17 Bray–
Curtis similarity
coefficient. 2D stress
level: 0.02.

The percentages of total variance explained by
the first three principal components (PCs) were
PC1 = 46%, PC2 = 24%, and PC3 = 15%. The
following cases had the highest contribution to the
variance of these PCs (Table 3): cephalopoda
(26%) to PC1; other fish (26%), juveniles of F.
californiensis (16%) and L. stylirostris (10%) to PC2;
and marine birds (14%) and cephalopoda (12%) to
PC3. The vaquita was among the first 10 cases that
contributed most to the variance of PC1, with a
contribution of 4.7%. The direction of the corre-
lation of each index with the first two PCs is plotted
in Figure 3; the projection arranges indices with
similar trends.
 Role of the Vaquita in the Northern Gulf of California 427

The indices with the most similar trends were

Figure 3. PCA based on correlations for the functional
groups and variables (A, R/B, TL, OI, Roi, B, P/B, P/Q, R, D,
and (ðA=CÞexti ) selected. The projection of the functional
groups shown as numbers and of the variables on the
plane of the two PCs that explain the major percent of
variance, reveal different groupings with similar roles
and hidden differences among the variables. See Table 2
for the identification key of the functional groups. The
vaquita position is highlighted in larger size.
plotted to examine the relationships between them
(Figure 4). A strong positive and significant corre-
lation was found between degree index (D) and
respiration (R) (Figure 4A), between biomass (B)
and R (Figure 4B), as well as between B and D
(Figure 4C) (Spearman rank correlation: rs = 0.99,
0.86, and 0.90, respectively; all P < 0.05). In all
cases, the groups with higher TL (for example,
California sea lion, vaquita, totoaba adults, odon-
toceti whales, marine birds) presented values lower
than those of groups with intermediate TL (for
example, cephalopods, fish, small pelagics, myc-
tophids), indicating that those species with greater
amounts of biomass in the ecosystem have higher
values of respiration and more trophic connections
of flow per group.
A correlation was also observed between TL and
ascendency (Figure 4D); although it was not as
strong as the previously observed correlations, it
was both positive and significant (rs = 0.72,
P < 0.05). This correlation suggests that groups
with higher TLs have greater values of ascendency
than groups with lower TLs (that is, shrimps, crabs,
and cephalopods). This result indicates that groups
in the upper level of the food web make major

Table 3. Relative Contribution Based on Correlations (%) of the Cases (Functional Groups) to the Variance of a PC
PC1 PC2 PC3

Case % Case % Case %

Cephalopoda 26.0 Other fish 25.7 Marine birds 13.9
Callinectes sp 8.5 F. californiensis (Juveniles) 15.8 Cephalopoda 12.4
Odontoceti 6.7 L. stylirostris (Juveniles) 10.3 Serranidae 8.9
Marine birds 6.2 Cephalopoda 9.4 Stomatopoda 8.6
Z. californianus 5.2 Small pelagics 7.0 L. stylirostris (Juveniles) 6.0
Small pelagics 5.1 F. californiensis (Adults) 7.0 Mojarras 6.0
Coastal birds 4.9 Myctophidae 5.3 S. penicillata 5.9
L. stylirostris (Juveniles) 4.7 L. stylirostris (Adults) 3.9 Haemulidae 5.6
P. sinus 4.7 Sharks 3.8 Rhinobatidae 5.4
Sharks 4.6 Callinectes sp 3.6 F. californiensis (Juveniles) 4.5
L. stylirostris (Adults) 3.8 Odontoceti 3.6 Odontoceti 4.3
T. macdonaldi (Adults) 3.6 Marine birds 1.5 Coastal birds 3.5
T. macdonaldi (Juveniles) 3.1 S. penicillata 0.9 Z. californianus 3.5
F. californiensis (Juveniles) 2.9 Rays 0.4 Flat fish 2.9
F. californiensis (Adults) 2.9 Flat fish 0.4 Rays 2.9
Other fish 2.5 Stomatopoda 0.3 P. sinus 2.0
Mysticeti 1.6 Coastal birds 0.3 Small pelagics 1.4
Myctophidae 0.8 Merluccidae 0.1 Sciaenidae 1.0
Merluccidae 0.7 Mysticeti 0.1 Sharks 0.4
Serranidae 0.4 Sciaenidae 0.1 Merluccidae 0.2
Mojarras 0.3 P. sinus 0.1 F. californiensis (Adults) 0.2
Flat fish 0.2 Serranidae 0.1 Callinectes sp 0.2
Stomatopoda 0.2 Z. californianus 0.1 Myctophidae 0.1
S. penicillata 0.2 Rhinobatidae 0.0 T. macdonaldi (Juveniles) 0.0
Rays 0.1 Mojarras 0.0 T. macdonaldi (Adults) 0.0
Sciaenidae 0.1 Haemulidae 0.0 L. stylirostris (Adults) 0.0
Haemulidae 0.0 T. macdonaldi (Juveniles) 0.0 Other fish 0.0
Rhinobatidae 0.0 T. macdonaldi (Adults) 0.0 Mysticeti 0.0

The values of the three PCs that explain the major percentages of variance are shown; the higher the contribution of a case, the heavier it weighs on the PC.
428 M. Riofrı́o-Lazo and others

contributions to the order of the ecosystem. The
correlation between the omnivory index (OI) and
the production/consumption ratio (P/Q) (Fig-
ure 4E) also appears to be positive and significant,
if not as strong (rs = 0.53, P < 0.05). Owing to a
dome-shape tendency perceived in the scatterplot,
it was adjusted to a quadratic function (coefficient
of determination: r2 = 0.4, P < 0.05). There is not
a clear explanation for the relationship between
these variables, with the exception that groups of
higher TL showed lower values of OI and P/Q than
those of lower TLs (that is, crabs, cephalopods, fish,
and small pelagics). These results suggest that the
lower the variability of a group’s diet, the lower is
its gross efficiency.
To represent the relationship between the pro-
duction/biomass ratio (P/B) and the role of a group
(Roi), we expressed both indices in a similar scale.
For Roi, we used its analog in information theory
eAMI, and for P/B its equivalent e-Z. As P/B is equal
to the total mortality Z in a population at equilib-
rium (Allen 1971) and is considered a function of
biomass and longevity, e-Z indicates the survival
rate or the survival performance within each
group. Figure 4F shows a negative exponential
relation between these variables, indicating that

Figure 4. Two-
dimensional scatterplot
visualizing the tendency
between the two closer
variables grouped in the
PCA. A Degree Index (D)
versus respiration (R), B
biomass (B) versus R, C B
versus D, D trophic level
(TL) versus ascendency
(A), E Omnivory Index
(OI) versus production/
consumption ratio (P/Q),
F production/biomass
versus role represented as
their equivalents: e-Z
versus eAMI, respectively.
The graphs were
generated with
standardized values. The
functional groups are
represented by numbers
inside the plots. The
vaquita position is
highlighted in larger size.
 Role of the Vaquita in the Northern Gulf of California
the lower the values of survival (e-Z), the higher
values of Roi (eAMI) for a group. The shrimps Calli-
nectes sp. and cephalopods showed higher values of
eAMI and lower values of e-Z than mysticetis, Cali-
fornia sea lions, sharks, vaquita, and totoaba. This
result indicates that most short-lived species play a
more relevant role in the ecosystem than the spe-
cies of long longevity. When considering in rela-
tionship to species role, these species contribute a
greater amount of information to the dynamics of
the system because of their greater flows.
DISCUSSION
The local extinction or large fluctuation in the
abundance of a species may seriously affect the
other species in its community (Jordán and others
2006). It is necessary to differentiate between spe-
cies that are important to nature (for example, for
maintaining ecosystem functions) and species that
may be more important to scientists or the general
public (for example, Red List species with limited
ecological roles). It is certainly important to protect
species of great esthetic or economic value, but it
should be recognized that they are protected for
reasons other than the maintenance of ecosystem
function (Simberloff 1998; Jordán 2009).
The degree index (D) is usually employed to
identify key species in the trophic web, those
that play a more important role than others in
structuring ecosystems due to their greater number
of links with other species in the inter-specific
interaction network (Jordán 2009). D gives a very
robust prediction on the positional importance of a
node and can be easily calculated with basic
information (Solé and Montoya 2001; Dunne and
others 2002). However, indicators of ecosystem
stability and stress, such as the indices of network
analysis, can provide a more accurate representa-
tion of the true ecological contribution of a species
(Ulanowicz 1986).
This is the first study that relates the emergent
network analysis indices (features of the ecosys-
tem) and the ecological attributes of the ecosys-
tem’s functional groups to measure the ecological
roles of these groups in the NGC ecosystem. In
general, our results suggest that the vaquita mainly
contributes to the order of the ecosystem in a
similar manner to other groups of apex predators,
such as coastal and marine birds, California sea lion
and the endangered totoaba. The ecosystem¢s order
is understood as the ascendency/development
capacity ratio, that is, the efficient/inefficient ratio
of energy use within the ecosystem. Other groups
were more closely related with ecosystem func-
429
tioning, such as shrimps (F. californiensis and L.
stylirostris), crabs (Callinectes sp., Stomatopoda), and
cephalopods as well as several species of fish,
myctophids, and small pelagics.
The mechanisms of trophic network control have
been studied for several years, and three primary
types of energy flow have been recognized (Matson
and Hunter 1992). These are top-down control
(control by predators), bottom-up control (control
by sources of energy or primary producers), and
wasp-waist control (control by dominant species of
intermediate TL, which exert both top-down con-
trol on lower TL and bottom-up control on top
predators) (Cury and others 2001; Hunt and
McKinnell 2006). However, an ecosystem is not
driven entirely by only one type of control but
instead by a subtly changing combination of them
that might depend on its state, diversity, and
integrity (Cury and others 2001). In the Gulf of
California ecosystem, small pelagic fish, mainly
sardines (Sardinops sagax caeruleus), are considered
to fulfil the wasp-waist function (Bakun and others
2010) because they constitute an important food
base for higher trophic level fish and other charis-
matic megafauna, such as sea lions (Garcı́a-Rodrı́guez
and Aurioles-Gamboa 2004) while also affecting
the TL below, which are fed upon by the wasp-
waist populations (Bakun and others 2010).
Our results suggest that the ecosystem of the
NGC is regulated by a wasp-waisted trophic con-
trol. The intermediate trophic level groups had the
highest values of degree index and large values of
keystone index (K), both of which suggest a func-
tion as controllers in the topology of the network.
In addition, the group with the highest trophic
level, sharks, had the highest K index value; the
odontoceti, vaquita, and California sea lion (groups
with higher trophic level) showed intermediate
values of the K index, which in turn indicated their
contribution to the maintenance and the structure
of the ecosystem.
With the exception of sharks and odontoceti,
those groups with higher TL showed the highest
values of development capacity and great values of
overhead, which are indicators of organization and
resilience (Ulanowicz 2002). This result indicates
the contribution of these groups to the develop-
ment and complexity of the ecosystem and its
sustainability sensu (Ulanowicz 2009). Alterna-
tively, functional groups with lower TL, such as
shrimp species and other crustaceans had the
highest values of overhead along with intermediate
values of development capacity.
A keystone species has a large impact on its
community, which is disproportionately large
430 M. Riofrı́o-Lazo and others
relative to its abundance (Power and others 1996).
Keystoneness is not an intrinsic property of a spe-
cies, but of its functional role in a particular com-
munity assemblage (Payton and others 2002). In a
network context, the keystone species plays a rel-
atively unique structural and functional role within
the network (Jordán 2009). The significance of this
unique pattern of interactions depends, among
other things, on the switching ability of species in
the ecosystem. If species are less opportunistic
consumers, organisms with unique interactions
may truly be candidate key species. In case of
highly aggregated networks, the links among large
trophic groups make the identification of key spe-
cies difficult (Jordán 2009). However, the model
used for the NGC has a good level of aggregation
with regards to the most important functional
groups of the ecosystem, allowing us to analyze the
role of the vaquita successfully (Lercari and
Arreguı́n-Sánchez 2008), namely, the contribution
of the vaquita to the ecosystem’s order and organi-
zation (based on Ulanowicz’s ascendency concept).
Moreover, in the NGC, Lercari and others (2007)
based on trophic interactions showed that the most
important predation effect on the vaquita is caused
almost exclusively by sharks; however, the preda-
tion role of vaquita is directed toward various
groups (small pelagics, serranidae, shrimps), sug-
gesting an opportunistic predation strategy (Pérez-
Cortés and others 1996). It is well known that life
history features can be important in the role that a
species plays; for example, resource limitation can
be an important factor in the population dynamics
of a species (Reznick and others 2002). The life
history features of the vaquita, such as its restricted
distribution, small effective population size, limited
genomic variability (Taylor and Rojas-Bracho
1999) and high vulnerability to incidental fishing
mortality, clearly suggest that we cannot expect it
to become a dominant species (Hohn and others
1996; Rojas-Bracho and others 2006). However,
due to its importance in ecosystem organization, it
is clearly an important indicator species, despite its
rarity (Rojas-Bracho and others 2006).
Through the analysis of Figure 3 from the PCA,
we found that the small pelagics and cephalopods
as well as other intermediate trophic level groups
showed similar tendencies in the direction of their
clustering vectors with variables such as biomass
(B), respiration (R), and the degree index (D).
Moreover, there was a strong relationship between
the pairs of variables D–R, B–R, and B–D. These
results suggest that groups of intermediate trophic
level (for example, cephalopods, other fish, small
pelagics, myctophids) have greater biomass in the
ecosystem, higher values of respiration, and more
connections of flow per group when compared to
groups of high and low trophic level.
On the other hand, the apex predators (notably
sharks, seabirds, and marine mammals, including
vaquita) had the highest values of ascendency and
ðA=CÞexti (the relative change in the ascendency
ratio calculated when group i is extracted of the
system). The extraction of a group shows the rela-
tive contribution of the group to the degree of
growth, organization, and development of a sys-
tem. Thus, our results indicate the contribution of
these groups to the order and sustainability of the
ecosystem. In the PCA, the apex predators showed
a greater correspondence with the ascendency (A)
and trophic level (TL). A strong positive correlation
was identified between these variables, suggesting
that the higher the trophic level of a group, the
higher its values of ascendency. Although the base
TL are more affected by events of perturbation, the
higher levels have more contribution to the degree
of ecosystem specialization and maturity.
Furthermore, groups from lower TL (that is,
shrimps and crabs) had higher AMI and higher role
(Roi) values than other groups, such as apex pre-
dators. Both indices are measures of the complexity
of the flow network. It is well known that AMI is
higher when the amount of material transferred is
concentrated through a few pathways, leaving
other existing pathways to transfer comparatively
small amounts (Allesina and others 2005). In
addition, each group plays a unique role in the
network, taking energy inputs from one source and
passing them onto another destination (Zorach and
Ulanowicz 2003). The results suggest that lower
trophic level groups play more important roles in
the organization and structure of flows than those
groups with higher TL, which include such groups
of high economic and conservation value, such as
sharks, seabirds, and marine mammals.
The shrimp species and other crustaceans
showed greater correspondences with variables
related to the metabolism: production/consump-
tion ratio (P/Q; gross efficiency), omnivory index
(OI; feeding behavior of the consumer groups),
production/biomass ratio (P/B; equivalent to the
mortality rate), and the role of a group (Roi; num-
ber of functions that occur in the network).
Although the correlation between OI and P/Q was
moderately strong, the OI versus P/Q plot suggests
that the lower trophic level groups, such as crabs,
cephalopods, fish, and small pelagics, which have
greater variability in the trophic positions of their
prey, transfer greater quanta of energy between
compartments in the network.
 Role of the Vaquita in the Northern Gulf of California
As observed above, there are complex interac-
tions among the functional groups of this ecosys-
tem. The vaquita, like other species of marine
mammals, aquatic birds, and some species of fish
with high trophic level, is an important contributor
to the maintenance, order, and sustainability of the
ecosystem due to its high values of ascendency and
ðA=CÞexti (relative change in the ascendency ratio).
These values also indicate that the vaquita makes
strong contributions to the maturity and special-
ization of the system. Furthermore, its higher val-
ues of overhead and development capacity indicate
a high contribution to the ecosystem recovery in
case of perturbations.
Ecosystem-based management assumes a rea-
sonable understanding of the interactions among
and between species complexes as well as the
interactions between species and their environ-
ment (Larkin 1996). The protection of species that
are structurally important in the ecosystem may
have greater direct and indirect positive effects on
ecosystem integrity and functioning. Nevertheless,
species of high economic or conservation value and
those which are well connected with them are also
important to protect and manage (Jordán 2009).
This study demonstrated the usefulness of the
applied approach for identifying the ecological role
of the groups in an ecosystem. The results sug-
gested a number of characteristics that should be
taken into account when setting future priorities
for sustainable ecosystem management such as: (1)
the major contribution to the organization and
structure of energy flows in the food web by the
lower trophic level groups (TLGs), (2) the control of
flows throughout the network by the intermediate
TLGs and (3) the contribution to the maintenance,
order and sustainability of the ecosystem mainly
displayed by the higher TLGs. All species groups
have important roles within the system because all
of them contribute to its organization. However,
certain groups develop specific functions to main-
tain proper order and functioning of the system and
to lead it to a greater degree of maturity and spe-
cialization over time. Even though the vaquita does
not demonstrate a remarkable or specialized role in
the system, it does contribute to the order of the
ecosystem as much as other species such as
Zalophus californiensis, Totoaba macdonaldii, and
marine birds (Figure 4D), but its functional role is
very limited as is shown by its biomass, respiration,
degree index (Figure 4A–C), and production/con-
sumption ratio (Figure 4E). However, it is highly
valued for its own sake and the analysis has helped
identify its role in ecosystem functioning which in
turn can be used for determining key aspects of the
431
ecosystem that may be managed to favor vaquita
conservation as much as possible.
Concerning management, two perspectives
related to conservation of the vaquita could be
considered; protection for a charismatic and
endangered species, and a policy of controlling
fishing coupled with the vaquita conservation
objective. Our results here offer some information
related to the role of the vaquita and other species
in the ecosystem, presumably useful for manage-
ment. In this sense, information provided will help
with understanding, but mostly, to support poten-
tial success of management measures.
Lercari and Arreguı́n-Sánchez (2008) explored
management balancing conservation and exploi-
tation of fish resources in the NGC. They consid-
ered eight local fleets: two industrial (trawling
shrimp), three artisanal targeting shrimp, and three
based on fish-gillnets. These authors estimated a
number of viable strategies aimed to compliment
both objectives, maintain fishing and conserve the
vaquita; where the viability is given, in addition to
the above objectives, by maintaining biomasses for
all groups between a range of 0.5 and 2.0 times the
initial biomass. In terms of fleets, this means the
reduction to 35% of the industrial shrimp fishery,
an increase in two of the three artisanal-shrimp
fleets by a factor of 2.4 (the third decrease 10%),
and the decrease of the three gillnet fleets at a level
of 45%. Diaz-Uribe and others (2012) studied the
upper half of the Gulf of California through a
model with nearly 180 functional groups and
indicate an important level of incidental fishing
mortality on the vaquita, as well as the loss of
habitat associated with the reduction of the flow of
the Colorado river; both human induced factors
yielding an equivalent of exploitation rate (F/Z) of
0.7, indicating the vaquita natural renewable rate
has been negatively affected. Lercari and others
(2007) suggest that the role of the existing marine
protected area is positive for the vaquita stock and
suggest improvements to this strategy.
Our results support the approach advocated by
Lercari and Arreguı́n-Sánchez (2008) of manage-
ment that balances conservation and exploitation
of fish resources in the NGC. They considered that
restricting the activity of industrial shrimp-trawling
fishing, the reduction of the industrial shrimp fleet
shifting by an increment of the artisanal-shrimp
fleets (a more selective fleet), results in an impor-
tant reduction of fishing mortality on shrimps and
also on shrimp-by-catch. These actions represent
an increase in biomass of low tropic levels that,
according to our estimations, are the groups with
higher contributions to the organization and
432 M. Riofrı́o-Lazo and others
structure of the ecosystem. Also, the reduction of
fishing by artisanal fleets indirectly benefits long-
lived species, mostly representing high tropic
levels, which have an important role in the main-
tenance of order in the ecosystem. From the
management point of view, the reduction of
uncertainty in management decisions is a key fac-
tor for the success of the measures. Even when we
do not quantify uncertainty, our findings about
the role of the species in the ecosystem suggest the
above measures contribute to the robustness of the
ecosystem in terms of structure, organization, and
function, which in turn give more certainty of
success to the measures proposed.
ACKNOWLEDGMENTS
The authors are thankful for the support received
from projects WWF (KH88), SEP-CONACyT
(104974, 155900), and SIP-IPN (20121417,
20121444) as well as from the Instituto Politécnico
Nacional through the EDI and COFAA programs.
FES thanks the Programa de Formación de Inves-
tigadores (PIFI) and the Consejo Nacional de
Ciencia y Tecnologı́a (CONACyT) for the scholar-
ship provided.
REFERENCES
Abarca-Arenas LG, Ulanowicz RE. 2002. The effects of taxo-
nomic aggregation on network analysis. Ecol Model 149:
285–96.
Allen KR. 1971. Relation between production and biomass. J
Fish Res Board Can 28:1573–81.
Allesina S, Bondavalli C, Scharler UM. 2005. The consequences
of the aggregation of detritus pools in ecological networks.
Ecol Model 189:221–32.
Alvarez-Borrego S. 2010. Physical, chemical, and biological
oceanography of the Gulf of California. In: Brusca RC, Ed. The
Gulf of California: biodiversity and conservation. Tucson: The
University of Arizona Press. p 24–48.
Aragón-Noriega EA, Calderón-Aguilera LE. 2000. Does dam-
ming of the Colorado River affect the nursery area of blue
shrimp Litopenaeus stylirostris (Decapoda: Penaeidae) in the
Upper Gulf of California? Revista de Biologı́a Tropical 48:867–
71.
Baird D, Ulanowicz RE. 1993. Comparative study on the trophic
structure, cycling and ecosystem properties of four tidal
estuaries. Mar Ecol Prog Ser 991:221–37.
Bakun A, Babcock EA, Lluch-Cota SE, Santora C, Salvadeo CJ.
2010. Issues of ecosystem-based management of forage fish-
eries in ‘‘open’’ non-stationary ecosystems: the example of the
sardine fishery in the Gulf of California. Rev Fish Biol Fish-
eries 20:9–29.
Brodziak J, Link J. 2002. Ecosystem-based fishery management:
what is it and how can we do it? Bull Mar Sci 70:589–611.
Brusca RC, Findley LT, Hastings PA, Hendrickx ME, Torre-Cosio
J, van der Heiden AM. 2004. Macrofaunal biodiversity in the
Gulf of California. In: Cartron JLE, Ceballos G, Felger R, Eds.
Biodiversity, ecosystems, and conservation in Northern
Mexico. New York: Oxford University Press. p 179–203.
Clarke KR. 1993. Non-parametric multivariate analyses of
changes in community structure. Aust J Ecol 18:117–43.
Clarke KR, Gorley RN. 2006. PRIMER v6: user’s manual/tuto-
rial. PRIMER-E: Plymouth, UK. p 192p.
Contreras-Balderas S, Almada-Villela P. 1996. Totoaba macdon-
aldi. In: IUCN 2007. IUCN red list of threatened species.
www.iucnredlist.org.
Cury P, Shannon L, Shin YJ. 2001. The functioning of marine
ecosystems. Reykjavik Conference on Responsible Fisheries in
the Marine Ecosystem. Reykjavik, Iceland
D’Agrosa C, Lennert-Cody C, Vidal O. 2000. Vaquita bycatch in
Mexico’s artisanal gillnets fisheries: driving a small population
to extinction. Conserv Biol 14:110–19.
Dı́az-Uribe JG, Arreguı́n-Sánchez F, Lercari-Bernier D, Cruz-
Escalona VH, Zetina-Rejón MJ, Del Monte-Luna P, Martı́nez-
Aguilar S. 2012. An integrated ecosystem trophic model for
the North and Central Gulf of California: An alternative view
for endemic species conservation. Ecol Model 230:73–91.
Dunne JA, Williams RJ, Martı́nez ND. 2002. Network structure
and biodiversity loss in food webs: robustness increases with
connectance. Ecol Lett 5:558–67.
Gallo-Reynoso JP. 1998. La vaquita marina y su hábitat crı́tico
en el Alto Golfo de California. Gaceta Ecológica INE-
SEMARNAP 47:29–44.
Garcı́a-Rodrı́guez FJ, Aurioles-Gamboa D. 2004. Spatial and
temporal variation in the diet of the California sea lion
(Zalophus californianus) in the Gulf of California, Mexico.
Fishery Bullet 102:47–62.
Gerrodette T, Taylor BL, Swift R, Rankin S, Jaramillo-Legorreta AM,
Rojas-Bracho L. 2011. A combined visual and acoustic esti-
mate of 2008 abundance, and change in abundance since
1997, for the vaquita, Phocoena sinus. Mar Mamm Sci 27:E79–
100. doi:10.1111/j.1748-7692.2010.00438.x.
Glen EP, Lee C, Felger R, Zengels S. 1996. Effects of water
management on the wetlands of the Colorado River Delta,
Mexico. Conserv Biol 10:1175–86.
Heymans JJ, Ulanowicz RE, Bondavalli C. 2002. Network anal-
ysis of the South Florida Everglades graminoid marshes and
comparison with nearby cypress ecosystems. Ecol Model
149:5–23.
Heymans JJ, Guénette S, Christensen V. 2007. Evaluating net-
work analysis indicators of ecosystem status in the Gulf of
Alaska. Ecosystems 10:488–502.
Hohn AA, Read AJ, Fernandez S, Vidal O, Findley LT. 1996. Life
history of the vaquita, Phocoena sinus (Phocoenidae, Cetacea).
J Zool 239:235–51.
Hunt GL, McKinnell S. 2006. Interplay between top-down,
bottom-up, and wasp-waist control in marine ecosystems.
Prog Oceanogr 68:115–24.
Jaramillo-Legorreta AM, Rojas-Bracho L, Gerrodette T. 1999. A
new abundance estimate for vaquitas: first step for recovery.
Mar Mamm Sci 15:957–73.
Jordán F, Liu WC, Davis AJ. 2006. Topological keystone species:
measures of positional importance in food webs. Oikos
112:535–46.
Jordán F. 2009. Keystone species and food webs. Philos Trans R
Soc Lond Ser B 364:1733–41.
Larkin PA. 1996. Concepts and issues in marine ecosystem
management. Rev Fish Biol Fisheries 6:139–64.
 Role of the Vaquita in the Northern Gulf of California
Lavı́n MF, Sánchez S. 1999. On how the Colorado River affected
the hydrography of the Upper Gulf of California. Cont Shelf
Res 19:1545–60.
Lercari D, Arreguı́n-Sánchez F, Le Quesne W. 2007. An eco-
system simulation model of the northern Gulf of California.
In: Le Quesne WJF, Arreguı́n-Sánchez F, Heymans SJJ, Eds.
INCOFISH ecosystem models: transiting from Ecopath to
Ecospace. Fisheries Centre Research Reports 15(6). Fisheries
Centre, University of British Columbia: Vancouver; [ISSN
1198-6727]. pp 100–113.
Lercari D, Arreguı́n-Sánchez F. 2008. An ecosystem modelling
approach to deriving viable harvest strategies for multispecies
management of the Northern Gulf of California. Aquatic
Conserv 19:384–97.
Lluch-Cota SE, Pares-Sierra A, Magaña-Rueda VO, Arreguı́n-
Sánchez F. 2006. Modeling climate change in the Gulf of
California. GLOBEC Int Newslett 12:70–1.
Lluch-Cota SE, Aragón-Noriega EA, Arreguı́n-Sánchez F,
Aurioles-Gamboa D, Bautista-Romero JJ, Brusca RC,
Cervantes-Duarte R, Cortés-Altamirano R, Del-Monte-Luna P,
Esquivel-Herrera A. 2007. The Gulf of California: review of
ecosystem status and sustainability challenges (Review). Prog
Oceanogr 73:1–26.
Matson PA, Hunter MD. 1992. Special feature: the relative
contributions to top-down and bottom-up forces in popula-
tion and community ecology. Ecology 73. p 723
Mageau MT, Costanza R, Ulanowicz RE. 1998. Quantifying the
trends expected in developing ecosystems. Ecol Model 112:1–22.
Nava-Romo JM. 1994. Impactos a corto y largo plazo en la
diversidad y otras caracterı́sticas ecológicas de la comunidad
béntico-demersal capturada por la pesquerı́a de camarón en el
norte del Alto Golfo de California. Dissertation, Instituto
Tecnológico y de Estudios Superiores de Monterrey, Mexico:
México.
Payton IJ, Fenner M, Lee WG. 2002. Keystone species: the
concept and its relevance for conservation management in
New Zealand. Sci conserv 203:29.
Pérez-Cortés H, Silber JK, Villa-Ramı́rez B. 1996. Contribución
al conocimiento de la alimentación de la vaquita, Phocoena
sinus. Ciencia Pesquera INP-SEMARNAP 13:66–73.
Piraino S, Fanelli G, Boero F. 2002. Variability of species’ roles in
marine communities: change of paradigms for conservation
priorities. Mar Biol 140:1067–74.
Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS,
Daily G, Castilla JC, Lubchenco J, Paine RT. 1996. Challenges
in the quest for keystones. Bioscience 46:609–20.
433
Reznick D, Bryant M, Bashey F. 2002. r- and K-selection revis-
ited: the role of density, resources, and environmental fluc-
tuations in life-history evolution. Ecology 83:1509–20.
Rojas-Bracho L, Jaramillo-Legorreta A, Gerrodette T. 2002. Are
aggregation behavior and local movements of vaquita
adversely influenced by fishing vessels? IWC Scientific Com-
mittee.
Rojas-Bracho L, Reeves RR, Jaramillo-Legorreta A. 2006. Conser-
vation of the vaquita Phocoena sinus. Mamm Rev 36:179–216.
Silber G, Newcomer P, Silber P, Pérez-Cortés H, Ellis G. 1994.
Cetacean of the northern Gulf of California distributions,
occurrence and relative abundance. Mar Mamm Sci 10:283–98.
Simberloff D. 1998. Flagships, umbrellas, and keystones: is sin-
gle-species management passé in the landscape area? Biol
Conserv 83:247–57.
Solé RV, Montoya JM. 2001. Complexity and fragility in eco-
logical networks. Proc R Soc B 268:2039–45.
Taylor BL, Rojas-Bracho L. 1999. Examining the risk of
inbreeding depression in a naturally rare cetacean, the vaquita
(Phocoena sinus). Mar Mamm Sci 15:1004–28.
Ulanowicz RE. 1980. An hypothesis on the development of
natural communities. J Theor Biol 85:223–45.
Ulanowicz RE, Mann KH. 1981. Ecosystems under stress. In: Platt
T, Mann KH, Ulanowicz RE, Eds. Mathematical models in bio-
logical oceanography. Paris: The UNESCO Press. p 133–7.
Ulanowicz RE. 1986. Growth and development: ecosystems
phenomenology. San Jose: Excel Press. 203 pp
Ulanowicz RE, Norden JS. 1990. Symmetrical overhead in flow
networks. Int J Syst Sci 1:429–37.
Ulanowicz RE, Abarca-Arenas LG. 1997. An informational syn-
thesis of ecosystem structure and function. Ecol Model 95:1–10.
Ulanowicz RE. 2001. Information theory in ecology. Comput
Chem 25:393–9.
Ulanowicz RE. 2002. Toward quantifying semiotic agencies:
habits Arising. J Semiotics Evol Energy Dev 2:38–55.
Ulanowicz RE, Goerner SJ, Lietaer B, Gómez R. 2009. Quanti-
fying sustainability: resilience, efficiency and the return of
information theory. Ecol Complex 6:27–36.
Vasconcellos M, Mackinson S, Sloman K, Pauly D. 1997. The
stability of trophic mass-balance models of marine ecosystems:
a comparative analysis. Ecol Model 100:125–34.
Zorach AC, Ulanowicz RE. 2003. Quantifying the complexity of
flow networks: how many roles are there? Complexity 8:68–76.