Ecological Indicators 110 (2020) 105866

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

The measurement of ecosystem development in Caribbean coral reefs T

through topological indices
⁎
Jimmy Argüelles-Jiméneza, , Jorge Christian Alva-Basurtob, Horacio Pérez-Españaa,
Manuel J. Zetina-Rejónc, Jesús Ernesto Arias-Gonzálezd
a
Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Hidalgo 617, Col. Río Jamapa, C.P. 94290 Boca del Río, Veracruz, Mexico
b
Parque Nacional Costa Occidental de Isla Mujeres, Punta Cancún y Punta Nizuc, Boulevard Kukulcán Km 4.8, Zona Hotelera, Municipio de Benito Juárez, C.P. 77500
Cancún, Quintana Roo, Mexico
c
Instituto Politécnico Nacional-Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politécnico Nacional S/N Col. Playa Palo de Sta. Rita, C.P. 23096 La Paz, BCS,
Mexico
d
Laboratorio de Ecología de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigaciones y de Estudios Avanzados del Instituto
Politécnico Nacional, Unidad Mérida, C.P. 97310 Mérida, Yucatán, Mexico

A R T I C LE I N FO A B S T R A C T

Keywords: The exploration of gradients of development stages of coral reef ecosystems is a subject poorly studied, especially
Development attributes when they exhibit multiple degrees of geomorphological or structural development or both. The objective of the
Succession present work was to study the gradient of functional and structural maturity of the Mexican Caribbean coral
Development stages reefs (CM). Here we analyzed three geomorphological zones that cover a gradient of 400 km in length in order to
Ecosystem maturity
obtain coral reefs with different geomorphologies. Thirteen reefs were selected, for which 12 ecosystem de-
Coral reefs
Mexican Caribbean
velopment attributes and five topological indices were analyzed. The development attributes of coral reefs were
estimated from trophic models constructed using Ecopath with Ecosim (EwE), while the topological indices were
calculated from the predator-prey matrix obtained from each EwE model. Through a partial redundancy analysis
(RDA) seven of the 12 development attributes (ascendency, overhead, development capacity, net primary
production, ascendency/development capacity, overhead/development capacity and richness of functional
group) were selected due their low or null collinearity. Using the developmental attributes selected in a non-
metric multidimensional scaling (stress: 0.1) and analysis of similarities (r global: 0.828 and p: 0.001), we found
a gradient of maturity that increases from north to south, i.e., northern coral reefs (e.g. Puerto Morelos) are less
mature than southern coral reefs (e.g. Mahahual). On other hand, through a non-parametric ANOVA and a
partial redundancy analysis (first axis: F-ratio = 62.054, p = 0.012; second axis: F-ratio = 1.591, p = 0.014;
100% of the total variance explained by the first two canonical axes) we detected that topological indices
respond to development stages, in this way the control flow increases with the maturity while the inter-
mediation, number of connections and number of interactions depredator-prey are inverse to maturity; there-
fore, topological indices can be used to describe development stages. The determination of a gradient of maturity
in MC coral reefs should be considered in management and conservation policies, therefore different strategies
must be implemented in ecosystems, because resilience and ecosystem response depend on them.

1. Introduction 2011) and despite having originated in the same geological period,
their geomorphological and structural development differs. This may be
The modern coral reefs located in the Caribbean Sea began their due to gradients of enviromental conditions (temperature, transpar-
development during the Holocene (Blanchon et al., 2002; Blanchon, ency, salinity, wave exposure, and hurricane impacts), which have a

Abbreviations: EwE, Ecoptah with Ecosim; NMDS, non-metric muldidimensional scaling; ANOSIM, analysis of similarities; SIMPER, percentage similarity analysis;
RDA, analysis of canonical redundance; Pp/R, primary production/respiration; Pp/B, primary production /biomass; TST, total system throughput; B/TST, biomass/
total system throughput; NPP, net primary production; A, ascendency; DC, development capacity; O, overhead; A/DC, ascendency/development capacity; O/DC,
overhead /development capacity; FCI, Finńs cycling index; S, functional diversity; Dc, degree centrality; Cc, closeness centrality; Bc, betweenness centrality; Dw,
weighted degree
⁎
Corresponding author.
E-mail addresses: cayix24@gmail.com (J. Argüelles-Jiménez), earias@cinvestav.mx (J.E. Arias-González).

https://doi.org/10.1016/j.ecolind.2019.105866
Received 21 July 2019; Received in revised form 22 October 2019; Accepted 24 October 2019
Available online 12 November 2019
1470-160X/ © 2019 Elsevier Ltd. All rights reserved.
J. Argüelles-Jiménez, et al. Ecological Indicators 110 (2020) 105866

direct effect on the fundamental biological processes (including meta-

bolites and photosynthesis) that determine the development of these
reefs. These gradients have been explained through the physicochem-
ical provinces described for the Caribbean Sea (e.g. Chollet et al.,
2012); in this way, a gradient of physicochemical regions with op-
timum, intermediate and suboptimal conditions for coral reefs exist in
the Caribbean Sea. An example of optimal conditions is the region of
the Inner Caribbean, with oligotrophic waters, far from large pluvial
discharges and characterized by stable warm environments, high
transparency, and low sedimentation. An example of reefs in the Inner
Caribbean, are those distributed throughout the Mexican Caribbean
(Chollet et al., 2012), and, for these reefs a decrease in geomorpholo-
gical development has been described from north to south (i.e., dif-
ferent reef extension, structural complexity, type and number of habi-
tats) (Gutiérrez-Carbonell et al., 1993, 1995; Arias-González, 1998;
Núñez-Lara et al., 2005). Some authors have identified differences in
the community structure of fish and corals in this area, as well as in the
geomorphological complexity and functioning of their trophic networks
(Núñez-Lara et al., 2005; Arias-González et al., 2011a; Rodríguez-
Zaragoza and Arias-González, 2015). Chávez and Hidalgo (1988) and
Chávez et al., (2007) have suggested that variations in reef geomor-
phology can result in differences in the level of ecosystem maturity.
Trophic structure is vital to understanding the structure and func-
tioning of ecological systems (Pimm et al., 1991). In this sense, Odum
(1969) argued that structural changes can occur in each ecosystem
development stage, being more complex in mature ecosystems. How-
ever, Odum (1969) did not delve into the structural behavior of trophic
networks, i.e., the role or importance of species and/or functional
trophic groups in the dynamics and structural stability of the eco-
system. For this reason and considering that the attributes of the eco-
systems provide a guide to understanding maturity gradients, the pre-
sent study intends to answer the following questions: 1) is there a Fig. 1. Study area. (A) Yucatan Peninsula. (B) North portion of the
gradient in the level of ecosystem development of coral reefs in the Mesoamerican Reef System and its three sectors. Thirteen reefs were selected
Mexican Caribbean that can be explained by geomorphological devel- for the study: Punta Nizuc (PN), Puerto Morelos (PMo), Punta Maroma (PMa),
opment? 2) Does the structure of trophic networks contrast with the Akumal (Aku), Boca Paila (BP), Yuyum (Yy), Punta Allen (PA), Punta Herrero
(PH), Tampalam (Ta), El Placer (EP), Mahahual (Ma), Xahuayxol (Xa) and
gradient of ecosystem development stages? In this last question, we
Xcalak (Xc). (C) Division of the reefs of the Mexican Caribbean based on their
explore the way in which topological indices characterize development
geomorphology: Northen sector (NS), Central sector (CS), and Southern sector
stages. Our approach is to determine the ecosystem’s maturity through (SS). Reef complexity with top and side view: L = lagoon, C = Cresta,
ecological networks analysis (ENA), using the ecological descriptors of F = front, S = slope, T = terrace. Depth in meters. Modified from Núñez-Lara
energy flows described by Odum (1969) and Ulanowicz (1986). et al., (2005), and Rodríguez-Zaragoza and Arias-González (2015).

2. Materials and methods

located in the southern sector (Núñez-Lara et al., 2005; Rodríguez-
Zaragoza and Arias-González 2015). For a detailed description of the
2.1. Study area
study area, see Arias-González (1998) and Arias-González et al.
(2011a).
The study area is located in the physicochemical province of the
Inner Caribbean (Chollet et al., 2012) and is part of the northern section
of the Mesoamerican Reef System, which has been considered one of 2.2. Ecopath models
the most biodiverse places in the Caribbean Sea (Arias-González et al.,
2011a). Thirteen reefs, located between 18°00′ and 21° 00′ N (Fig. 1) Models analyzed were built using the Ecopath with Ecosim software
were selected, which are part of a semicontinuous fringing reef that (EwE v6.5; available at http://www.ecopath.org). The EwE approach is
grows near and parallel to the coast, from Cancun to the border be- defined by a linear equation for each species or functional group (i)
tween Mexico and Belize (Arias-González et al., 2011a; Alba-Basurto included in the model. Each equation represents an energy balance
and Arias-González, 2014; Rodríguez-Zaragoza and Arias-González, between production and energy costs. Therefore, the output of each
2015). According to its geomorphological characteristics, current group (i) can be expressed by the linear Eq. (1):
human developments and patterns of use and protection, the reefs can n
P
be grouped into three sectors (north, center and south). The northern Bi ∗ ⎛ ⎞ ∗ EEi − ∑ Bj ∗ ⎛ Q ⎞ ∗ DCji − Yi − Ei − BAi = 0
sector includes Punta Nizuc (PN), Puerto Morelos (PMo), Punta ⎝ B ⎠i j=1 ⎝ B ⎠j (1)
Maroma (PMa), and Akumal (Aku) reefs. These reefs are characterized P
where for a group i , Bi is the biomass, is the production/biomass
by two habitats (lagoon and forereef) with long discontinuous and Bi
continuous coral formations, separated by large expansions of sand. On ratio, EEi is the ecotrophic efficiency, Bj is the predator biomass j, Q is
Bi
the other hand, the reefs of the central and southern sector have four the consumption/biomass relationship of the predator j , DCji is the
habitats (lagoon, forereef, slope and terrace), and have more developed fraction of i in the diet of j , Yi is the export value or fishing catch of
structures with spur and groove systems. The Boca Paila (BP), Yuyum group i, Ei is the net migration rate (emigration-immigration) and BAi is
(Yy), Punta Allen (PA), and Tampalam (Ta) reefs are in the center while the rate of accumulation of biomass. These last two elements were not
El Placer (EP), Mahahual (Ma), Xahuayxol (Xa), and Xcalak (Xc) are used in the present study due to the lack of data and assuming that the

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J. Argüelles-Jiménez, et al.
net balance of migration and accumulation of biomass is insignificant.
For each equation of each group i, input parameters include B, P/B, Q/B
and EE as well as the composition of the diet (DCij ) of all consumers. At
least three of the four basic parameters for each functional group of the
model must be included, and the program can calculate the remaining
value through the EE. The EE is the proportion of the production that is
used within the system and must be less than or equal to 1; usually the
EE is used to check the balance of the model. Fishing values may or may
not be included, depending on the presence of a fishing fleet
(Christensen et al., 2008).
2.3. Construction of the models
Input data were collected from the beginning of the year 2000, and
are based on fish counts and benthic records in the study area (Núñez-
Lara et al., 2005; Arias-González et al., 2004; Acosta-González et al.,
2013) using linear transects of 50 × 2 m carried out in 714 sites dis-
tributed among the 13 reefs. At each site 12 replicates were performed,
and number and length of the fish was recorded. Fish length was con-
verted into biomass using length-weight relationship for which the
parameters were obtained from samplings performed in this area
(Arias-González et al., 2004), and from electronic FishBase database
(Froese and Pauly, 2019). Biomass of functional groups that were not
fish were estimated by EwE.
Both the aggregation of functional groups of similar ecological
characteristics (Table 6) as well as diet values for non-fish groups were
based on Opitz (1996). The basic parameters of production/biomass (P/
B) and consumption/biomass (Q/B) for the fish groups were obtained
from FishBase (Froese and Pauly, 2019). The values of the diet matrix
and P/B were adjusted gradually for each of the models until they were
balanced, when all EE < 1. The fishing values were obtained from
commercial catch data (in tonnes) was obtained from a goverment of-
fice dedicated to monitoring fishing in Mexico (Secretaria de Agri-
cultura, Ganadería, Desarrollo Rural, Pesca y Alimentación: SAGARPA)
in the state of Quintana Roo.
For each model biomass data were standardized at t/km2 and
evaluated with a prebalance (PREBAL; Links, 2010). This diagnosis
provides a guide (Table 7) that was used to identify problems related to
the structure of the model and quality of the data after the mass balance
(Links, 2010).
2.4. Theory/calculation
2.4.1. Ecosystem development stages
For each of the 13 models, 12 ecosystem attributes were quantified.
Odum (1969) and Ulanowicz (1986) proposed eleven attributes to de-
scribe the ecosystem development stages and one additional attribute
was proposed by the authors of the present study (net primary pro-
duction, see Table 1). Development attributes can be cataloged in two
of the six categories proposed by Odum (1969): 1) community en-
ergetics, and 2) community structure. Although species richness is
found in the category of community structure, we propose to use
functional diversity (S) instead, because functional trophic groups have
the potential to generate a better approach to describe process that
occur within an ecosystem (Abarca-Arenas and Ulanowicz (1986));
even if two ecosystem have the same number of species, they will not
necessarily have the same number of functional groups, so each eco-
system will tend to function differently. Table 1 briefly describes at-
tributes of the ecosystems used.
To establish the developmental stages of the Mexican Caribbean
coral reefs, the development attributes that contributed to explaining
the gradient of maturity and that did not present colinearity were se-
lected (Table 8); this selection was carried out using forward selection
in a partial redundancy analysis (Ter Braak, 2002). For this, the geo-
morphological gradient of the Mexican Caribbean (factored) was con-
sidered the response variable and the 12 normalized development
3
Ecological Indicators 110 (2020) 105866
attributes were considered the predictor variables. The significance of
the final model that validated the selected development attributes was
evaluated through a Monte Carlo test with 9999 permutations.
The development stages (groups) were established with the selected
development attributes by means of non-metric multidimensional
scaling (NMDS). To test if the groupings established through the NMDS
differ significantly, a one-way analysis of similarity (ANOSIM) was
applied, and, the classification of the developmental stages obtained
from the NMDS was used as a factor. On the other hand, to evaluate the
contribution of the development attributes to each grouping, a per-
centage similarity analysis (SIMPER) was applied to identify those
variables that contributed to 95% of the cumulative contribution. As a
measure to reduce variation of out-lier data, developmental attributes
were normalized before performing the NMDS, ANOSIM and SIMPER.
Both the NMDS and the ANOSIM were performed on a dissimilarity
matrix estimated using the euclidean distance. The three analyses were
carried out with the PRIMER-E v7 software (Clarke and Gorley, 2006).
2.4.2. Structural analysis
In a trophic network, not all functional groups are equally relevant
in terms of structural dynamics and stability, hence their importance
can be quantified by analyzing the contribution of each group and as a
whole; this can reveal general structural patterns (Abascal-Monroy
et al., 2015). Considering this last idea, four topological indices (degree
centrality, closeness centrality, betweenness and weighted degree) and
one of substructures (modularity) were calculated using the consump-
tion matrix estimated by EwE and transformed to log10 (Abascal-
Monroy et al., 2015; Zetina-Rejón et al., 2015). Each index was nor-
malized to allow the comparison of results between models. Topolo-
gical indices and their normalization were performed using the igraph
library (Csardi, 2017) in R software (R Development Core Team, 2018).
Topological indices are briefly described below:
a) Degree centrality (Dc ), considers the number of connections or re-
lationships of the functional groups (prey and predators), so that the
functional groups with the greatest number of connections are ob-
tained (Wasserman and Faust, 1994; Allesina et al., 2009).
b) Closeness centrality (Cc ), measures the average of the inverse of the
distance between a given functional group and the rest of the
functional groups in the network; high values indicate a close re-
lationship between the given group and the other groups in the
trophic network (Wasserman and Faust, 1994).
c) Betweenness centrality (Bc ), quantifies the frequency at which a
functional group appears in the trophic routes between each pair of
groups in the trophic network (Wasserman and Faust, 1994). In
other words, it measures the importance of a functional group that
appears frequently in trophic routes and that presents a position in
the flow of matter from one group to another, or from one trophic
level to another (Abarca-Arenas et al., 2007).
d) Weighted degree (Dw ), is given by the sum of the flow of magnitudes
between a functional group in terms of its position in the trophic
network and in terms of the energy that flows through it (Horvath,
2011), i.e. it measures the control that a functional group has over
the flow of energy among the rest of the functional groups.
e) Modularity, unlike the topological indices, which are estimated for
each functional group, this indicator measures the degree to which
the trophic network is structured in subgroups (groupings). These
subgroups are characterized because members that compose them
have more intense trophic interactions with each other than with
other groups in the trophic network (Stouffer and Bascompte, 2011;
Zetina-Rejón et al., 2015). The modularity of each model was
quantified by means of the algorithm “fast-greedy finding”
(Newman and Girvan 2004), which is included in the igraph library
(Csardi, 2017). This algorithm uses modularity as a function of
maximization in an iterative way. Considering that modules are
groups determined by the strength of their trophic interactions,
J. Argüelles-Jiménez, et al. Ecological Indicators 110 (2020) 105866

Table 1
Development attributes used to assess development stages of the Mexican Caribbean coral reefs. References: Odum (1969)1, Ulanowicz (1986)2, Reaka-Kudla
(1997)3, Chollet et al. (2012)4 and Robertson et al. (2014)5.
Attribute Description Development stages Maturity stage

Primary production/respiration Relationship between primary production and the respiration rate. >1 ∼1
(Pp/ R )1
Primary production /Biomass Relationship between primary production and the total biomass. Lower Higher
(Pp/ B ) 1
Total system throughput (TST ) 2 Measurement of the metabolism of the system that describes its size and vigor. Lower Higher
Biomass/ Total system throughput Relationship between the total biomass of the system with respect to the TST . Lower Higher
(B / TST )1
Net primary production (NPP ) In mature ecosystems there is an increase in TST 1, which must be supported by various sources, Lower Higher
such as net primary production. It is proposed that this measure is positively associated with the
metabolism of the system and with energy cycling.
Ascendency ( A )2 Measurement of the size and maturity of the organization of flows in the ecosystem. Lower Higher
Development capacity (DC )2 Describes the full potential for the development of an ecosystem. Lower Higher
Overhead (O )2 The amount of DC that does not appear as an organized structure and that is available to be Lower Higher
organized as the system develops.
A/ DC 2 Relationship between A and DC that describes the degree of specialization. Lower Higher
O/ DC 2 Relationship between O and DC that describes the resilience of the system. Higher Lower
Finńs cycling index (FCI )1,2 The fraction of the total transfers of the system that is cycled. Lower Higher
Functional diversity (S ) Species diversity increases in succession processes and decreases in mature stages, with exception Lower Higher
of forests1. Coral reefs have a great species diversity3 that are housed in the inert structures (e.g.
CaCO3 in the reefs, wood in forests) that maintain their developed configurations. The greatest reef
fish diversity coincides with the Inner Caribbean4,5, which is composed of physicochemical
provinces where optimum values for the proper development of coral reefs are presented. Here it is
proposed that number of functional groups behaves as species diversity tends to increase towards
mature ecosystems, thus helping ecological redundancy and ecosystem stability.

these were used as a factor to determine whether the topological

indices differ between reefs and stages of development; the modules
were identified by their average trophic level (i.e. low, intermediate
and high).

Finally, to establish whether the topological indices differ between

the development stages, a nonparametric ANOVA was applied using the
Kruskal-Wallis test. The factor in each ANOVA performed was the
classification of the development stages obtained from the NMDS and
ANOSIM. As a complement to the Kruskal-Wallis test and to identify
association trends between the topological indices, the average trophic
level (number of modules per reef) and the development stages, a
partial redundancy analysis (RDA) was carried out. For this, the matrix
of topological indices were related to a factorial matrix (average trophic
level of the modules), while the development stages were used as a
supplementary variable. Prior to the RDA analysis, the topological in-
dices were normalized, and their significance was tested using the Fig. 2. Nonmetric multidimentional scaling (NMDS) based on the Euclidean
Monte Carlo test with 9999 permutations. The nonparametric ANOVA distance for seven development attrbutes: A , O , DC , NPP , A/ DC , O/ DC and S .
was carried out in R (R Development Core Team, 2018) and the RDA The code of the reefs corresponds to Fig. 1; High_D: high development, Med-
ium_D: intermediate development and Low_D: low development.
was performed using the CANOCO software (Ter Braak, 2002).

Table 2
3. Results
One-way comparisons through the ANOSIM between the development stages
identified considering the development attributes.
3.1. Ecosystem development stages
Comparisons R P

Five (PP/B, B/TST, PP/R, TST and FCI) of 12 attributes of devel- Global 0.828 0.0001
opment ecosystem, were discarded because they presented high coli- Low vs medium 0.606 0.008
nearity and had little explanatory power (Table 8), therefore the final Low vs High 0.994 0.008
model of the partial RDA with the nine remaining development attri- Medium vs High 0.979 0.029

butes was significant (first axis: F-ratio = 5.319, p = 0.0397; second

axis: F-ratio = 2.642, p = 0.0423; 100% of the total variance explained
attributes appeared in all three groups. Attributes that contributed most
by the first two canonical axes). With the remaining attributes, the
to the formation of the groups were A/DC, O/DC and S, while the at-
NMDS detected three groups of development stages, which coincide
tributes O, DC, NPP and A contributed less (Table 3). A characteristic of
with the three geomorphological sectors of the Mexican Caribbean: 1)
the attributes NPP, A, O and DC is that they presented low internal
north: low development, 2) center: intermediate development and 3)
variation and clearly distinguish the three stages of development, which
south: high development (Fig. 2). ANOSIM results indicated that there
is contrary to what the attributes A/DC, O/DC and S exhibit by partially
are significant differences between the three groups (Table 2).
distinguishing some of the stages of development and presenting
The SIMPER at 95% indicates that although the order of importance
greater internal variation (Fig. 3).
of the attributes is different between the development stages, the same

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J. Argüelles-Jiménez, et al. Ecological Indicators 110 (2020) 105866

Table 3
Percentage Similarity Analysis (SIMPER) with a 95% contribution for the development attributes in three ecosystemic development stages.
Low development Medium development Hight development

DA Mean Co AC DA Mean Co AC DA Mean Co AC

1 1 1
A/DC 22.43 25.62 25.6 S 41 22.26 22.3 S 41.3 26.46 26.5
O/DC1 77.57 25.62 51.2 O/DC1 77.59 18.34 40.6 A/DC1 22.51 22.15 48.6
S1 37.4 13.27 64.5 A/DC1 22.41 18.34 58.9 O/DC1 77.5 22.15 70.8
O2 24,030 8.89 73.4 O2 38,466 10.32 69.3 A2 23,302 7.35 78.1
DC2 30,981 8.88 82.3 DC2 49,579 10.29 79.6 NPP2 8006 7.32 85.4
NPP2 2389 8.87 91.2 NPP2 3813 10.26 89.8 DC2 103,511 7.29 92.7
A2 6951 8.85 100 A2 11,114 10.19 100 O2 80,209 7.27 99.99

DA: Development attributes, Mean: average of each development attribute, Co: contribution (%), AC: accumulated contribution (%). The superscript 1 is for the
attributes that partially distinguish development stages, while 2 is for those that distinguish them clearly based on the boxplots in Fig. 3.

3.2. Structural analysis
The Kruskal-Wallis test detected that the topological indices (Dc , Cc ,
Bc , WD ) discern the different stages of development (Fig. 4). One of the
four topological indices, Cc , indicates that the interactions (depredador-
prey) among functional groups tends to be greater for less developed
ecosystems (H = 284.03, p < 0.0001). Contrary to Cc , WD , which
determines the intensity of the connections in terms of energy flow,
tends to increase in reefs of greater ecosystemic development
(H = 9.69, p = 0.0079). On the other hand, Dc and Bc did not show
significant differences between the three development stages
(H = 0.86, p = 0.64 and H = 1.24, p = 0.49, respectively).
Finally, the RDA corroborates the trends described at the develop-
ment stage level and demonstrates the importance of the average
trophic level analyzed through the modules (Fig. 5). In this way, the
highest values of DW occur in reef ecosystems with greater ecosystemic
development (except for Punta Nizuc), linked to the intermediate and
high trophic levels. On the other hand, the highest values of Dc and Bc
were associated with low and intermediate development stages and a
high average trophic level (e.g. Punta Maroma, Yuyum reefs), while Cc
presented a negative relationship with the ecosystems of greater eco-
systemic development (e.g. Mahahual) and tended to be independent of
the trophic level.

Fig. 3. Box plot of the attributes of three stages of development identified in the reefs of the Mexican Caribbean. NPP : net primary production, A : ascendency, O :
overhead, DC : development capacity, A/ DC : ascendency/developmente capacity, O/ DC : overhead/development capacity and S : diversity of trophic groups.

5
J. Argüelles-Jiménez, et al.
Fig. 4. Box plot of the topological indices in three stages of development identified in the reefs of the Mexican Caribbean. Dc = degree centrality, Cc = closeness
centrality, Bc = betweenness centrality, WD = weighted degree. Different letters indicate significant differences.
Fig. 5. Canonical Redundancy Analysis (RDA) between the topological indices,
the average trophic level per reef and the ecosystem development stages of the
Mexican Caribbean reefs (first axis: F-ratio = 62.054, p = 0.012; second axis: F-
ratio = 1.591, p = 0.014; 100% of the total variance explained by the first two
canonical axes). The dark blue arrows indicate the topological indices:
Dc = degree centrality, Cc = closeness centrality, Bc = betweenness centrality,
WD = weighted degree. The sky-blue arrows indicate the average trophic level
per reef (LTL: low trophic level, ITL: intermediate trophic level, HTL; high
trophic level): Punta Nizuc (PN), Puerto Morelos (PMo), Punta Maroma (PMa),
Akumal (Aku), Boca Paila (BP), Yuyum (Yy), Punta Allen (PA), Punta Herrero
(PH), Tampalam (Ta), El Placer (EP), Mahahual (Ma), Xahuayxol (Xa) y Xcalak
(Xc). The gray arrows denote the development stage (LD: low development, ID:
intermediate development; HD: high development).
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Ecological Indicators 110 (2020) 105866
4. Discussion
4.1. Ecosystem development stages of the Mexican Caribbean coral reefs
Studies that analyze development attributes in Caribbean Sea coral
reefs are scarce, especially those that use models built with similar
criteria (e.g. Arias-González, 1998; Cobián et al., 2017). From an eco-
logical point of view, the construction of models following the approach
of Opitz (1996) can be considered appropriate since it is based on a
good number of functional groups (and species that integrate them)
which considers the size of the species, their metabolic rates and
trophic similarities. In the definition of trophic groups such attributes
have been considered of vital importance for the construction of eco-
logical models, since they generate a better approximation to describe
the processes that occur within an ecosystem (Abarca-Arenas and
Ulanowicz, 2002; Pinnegard et al., 2005). In this context, the present
study is the first to analyze development gradients for the coral reef
ecosystems in the Caribbean Sea under the same ecological construction
scheme. The statistical methods used RDA, NMDS, ANOSIM and
SIMPER helped to address the maturity gradient, and showed that the
geomorphological sectors of the Mexican Caribbean with differences in
the community structure of fish and corals (e.g. Núñez-Lara et al., 2005;
Arias-González et al., 2008; Arias-González et al., 2011a; Rodríguez-
Zaragoza and Arias-González, 2015) have different stages of develop-
ment. In this way, as the geomorphological and/or structural com-
plexity of the reefs increases towards the south of the Mexican Car-
ibbean, the diversity (Arias-González et al., 2011a), functional diversity
and maturity of the coral reefs also increase.
4.1.1. Comparison with existing evidence from literature
Legendre (1993) and Legendre and Legendre (2003) suggested that
J. Argüelles-Jiménez, et al. Ecological Indicators 110 (2020) 105866

Table 4
Comparisons of the ecosystem development attributes with studies conducted on Caribbean Sea reefs.
Categories DA Low development Medium development High development

LDP LGu IDP Ma G&G HDP Ta BP ML IV CCo

G1 PP/R(∼1) 1.031 2.56 1.031 1.25 1 1.03 1.27 1.28 1.6 1.26 5.78
PP/B(+) 8.62 18.28 8.56 12.45 24.33 8.69 14.08 15.6 10.21 – 11.82
B/TST (+) 0.041 0.021 0.041 0.025 0.009 0.04 0.022 0.021 0.036 0.047 0.038

G2 TST(+) 6,803 3,275 10,860 13,169 14,332 22,804 45,202 48,037 71,305 107,473 220,232
NPP(+) 2,389 1,249 3,813 4152 3118 8,006 14,293 15,889 26,043 20,025 98,796
A(+) 6,951 4,095 11,114 18,802 – 23,302 54,142 55,578 96,334 147,524 296,771
O(+) 24,030 8,079 38,466 37,812 – 80,209 105,380 122,523 218,036 290,689 331,127
DC(+) 30,981 12,174 49,579 56,615 – 103,511 159,523 178,101 314,370 438,213 627,897

G3 A/DC(−) 22.43 33.64 22.42 33 – 22.51 34 31 31 33.7 47

O/DC(−) 77.57 66.3 77.59 67 – 77.49 66 69 69 66.3 53
FCI(−) 7.39 7.47 7.4 13.6 – 7.43 14.3 11.7 6.95 18.3 1.6
S(+) 37.4 27 41 13 51 41.3 13 13 21 50 22

DA = Development attributes; G1 = Group one of DA, G2 = Group two of DA, G3 = Group three of DA; LDP = average of the DA for the reefs with a low devel-
opment stage in the present study, LGu7 = La Guajaira (Críales-Hernández et al., 2006), IDP = average of the DA for the reefs with an intermediate development
stage in the present study, Ma = Mahahual (Arias-González 1998; Arias-González et al., 2004), G&G = Grenada and Grenadines (Mohammed 2003), HDP = average
of the DA for the reefs with the highest development stage in the present study, Ta = Tampalam - BP = Boca Paila (Arias-González 1998; Arias-González et al., 2004),
ML = Media Luna - CCo = Cayos Cochinos (Cáceres et al., 2015), VI = Virgin Islands (Opitz 1996).

autocorrelation is a property of gradients, so, in order to increase the
knowledge of coral reef ecosystem development, all 12 development
attributes are analized irrespective of whether or not the attributes
present collinearity.
Through statistical analyses used, we distinguish three groups of
development attributes: G1) those which have low explanatory power
and high colinearity (PP / R , PP / B , B / TST ); G2) those that help to se-
parate development stages (NPP , A , O , DC ), and G3) those that par-
tially separate development stages ( A/ DC , O/ DC , S ) (Table 4). Since
TST is colinear with A (Table 8), it is included in G2, although for the
FCI the authors suggest including it in G3 because it could separate
partially stages. On the other hand, we expected that G1 attributes help
to discern gradients at a large geographic scale, as long as the same
criterion of ecological construction is used and ecosystems with marked
variations in their geomorphological development are included.
Through the three groups of attributes and the development stages
identified, comparisons can be made with other studies (Table 4) to
denote trends in the degree of maturity. Considering the values of the
G2 attributes, La Guajaira is considered a reef with low development,
Grenada and Grenadinas with intermediate development, while Media
Luna, Cayos Cochinos and Virgin Islands denote greater maturity.
However, these comparisons should be considered with caution (except
for the study carried out in the Virgin Islands), because construction
criterion and number of functional groups differ, which affects the re-
sults of each study. By example, studies that have addressed develop-
ment attributes for the Mexican Caribbean coral reefs (Arias-González
1998; Arias-González et al., 2004), describe an inverse trend, i.e., a
lower ecosystem development stage for southern coral reefs such as
Mahahual and a higher stage for the northern reefs, such as Boca Paila
reef (Table 4).
These contradictory results may be due to the construction criterion
used and the smaller number of functional groups, which are close to
the limit (n = 12) suggested by Louis-Félix and Sugihara (1997) to re-
present an ecosystem. Different studies (e.g. Abarca-Arenas and
Ulanowicz 2002; Krause et al., 2003; Heymans et al., 2014) have
pointed out that both the construction criterion and the number of
functional groups influence the final values of the development de-
scriptors (e.g. A , O and DC ) and the detectability of substructures such
as modules (Krause et al., 2003). Therefore, it is necessary to standar-
dize the criterion of ecological construction to give certainty to these
comparisons, since incorrect conclusions could be made regarding the
ecosystem development stages of the Caribbean Sea reefs.
4.2. Topological indices and development stages
Coral reef ecosystems contain a great diversity (Reaka-Kudla, 1997)
that is reflected in the complexity of their trophic interactions. Al-
though Odum (1969) suggests that structural complexity increases in
mature ecosystems, the dynamics and structural stability in the process
of functional development and maturity are unknown. Considering the
information gaps, we use topological indices in trophic networks, be-
cause, they have different applications, such as identifying key ecolo-
gical roles (e.g. Sole and Montoya, 2001; Bauer et al., 2010), as well as
global temporal (Abascal-Monroy et al., 2015) or spatial patterns. In the
spatial sense, topological indices helped to test the hypothesis that
suggests the existence of differences in the structure of trophic networks
due to a spatial geomorphological gradient, which is related to different
ecosystem development stages. Likewise, through exploration of topo-
logical indices we find two trends. First trend indicates that Cc and DW
indices can differentiate development stages, so, they are proposed as
developmental attributes. In the second trend, Dc and Bc indices only
denote differences when analyzed together with average trophic level
of the modules and development stages, i.e., the response of these in-
dices is masked by trophic level of their substructures (modules).
Considering that modules are influenced by the strength of trophic in-
teractions (Stouffer and Bascompte 2011; Zetina-Rejón et al., 2015),
their application to describe the importance of trophic levels in the
topology of networks helped to discern the patterns found. On the other
hand, a greater number of modules in reefs considered mature or HD
(Table 5) implies greater stability and persistence of their trophic net-
works, as suggested by Pimm (1979) and Stouffer and Bascompte
(2011).
4.2.1. Comparison with existing evidence from literature
Although trends described in Section 4.2 are clear, it is not possible
to delve into other reef systems of the Caribbean Sea because there are
no published studies integrating topological indices and development
attributes. Studies that address topological indices and development
attributes to a certain extent are those carried out in coastal lagoons
(Table 5), ecosystems that according to various studies, such as
Heymans et al., (2014) and those shown in Table 5, are inmature be-
cause they have low TST values. Despite the information gaps, the in-
formation analyzed in Table 5 helps to explain and theorize patterns.
In relation to Cc and DW , these were found to describe inverse
trends, i.e., Cc increases in ecosystems with low development while DW
increases in reefs with high development. The Cc index indicates that in

7
J. Argüelles-Jiménez, et al. Ecological Indicators 110 (2020) 105866

Table 5
Comparisons of development attributes and topological indices with studies carried out in coastal lagoons.
Categories DA LDP TLa-1980 TLa-1998 TLa-2011 BMa IDP HDP

G1 PP/R(∼1) 1.031 6.17 3.98 4.49 1.14 1.03 1.03

PP/B(+) 8.62 – – – 9.26 8.56 8.69
B/TST (+) 0.041 0.07 0.06 0.07 – 0.041 0.04

G2 TST(+) 6,803 4,926 2,972 2,080 3,361 10,860 22,804

NPP(+) 2,389 – – – – 3813 8006
A(+) 6,951 5,918 3,667 2,598 – 11,114 23,302
O(+) 24,030 9,014 6,704 4,445 – 38,466 80,209
DC(+) 30,981 14,932 10,371 7,025 – 49,579 103,511

G3 A/DC(−) 22.43 39.63 35.36 36.98 22 22.42 22.51

O/DC(−) 77.57 60.37 64.64 63.28 – 77.59 77.49
FCI(−) 7.39 3.04 4.32 3.65 – 7.4 7.43
S(+) 37.4 40 40 40 30 41 41.3

Topological indices Cc All ITL ITL ITL ITL All All

Bc HTL – – – ITL HTL HTL
Dc HTL – – – ITL HTL HTL
DW ITL LTL LTL LTL/ITL – ILT ITL/HTL
Modules 3 – – – – 3 3.5

DA = Development attributes; G1 = Group one of DA, G2 = Group two of DA, G3 = Group three of DA; LDP = average of the DA for the reefs with a development
stage in the present study, IDP = average of the DA for the reefs with an intermediate development stage in the present study, HDP = average of the DA for the reefs
with the highest development stage in the present study; TLA = Terminos Lagoon (Abascal-Monroy et al., 2015), BMa = Bahía Magdalena (Cruz-Escalona et al.,
2016); All = high values at all trophic levels, HTL = high trophic level, ITL = intermediate trophic level, LTL = low trophic level.

reefs with low development there is easy access to other members of the
trophic networks, which may be due to fewer low complexity habitats
(Arias-González et al., 2011a), which generate a smaller number of
spaces and structures for protection against predators; as a con-
sequence, all trophic levels (based on the modules) have a high and
similar access to the members of the networks. It has been shown that
when the complexity and number of habitats increase, the vulnerability
of prey to predators is reduced (Claro et al., 1990; Cobián et al., 2016,
2017), resulting in reduced access to members of the community net-
work and a greater richness and abundance of fish, as occurs in the
south of the Mexican Caribbean (Núñez-Lara et al., 2005; Arias-
González et al., 2011a). This trend is not the same in coastal lagoons
with low development (Table 5), possibly due to two factors: 1) dif-
ferent ecological processes: for example, high productivity results in the
greatest access to members of the network through intermediate trophic
levels that interact strongly with higher and lower trophic levels
(Abascal-Monroy et al., 2015; Cruz-Escalona et al., 2016), and 2) the
maturity scale; it is important to consider that the G1 attributes of the
Mexican Caribbean tend to be similar in the three development stages
of the reefs studied. Therefore, if these attributes are useful at a large
development scale, then, theoretically, reefs can ocurr with even lower
development stages than that described for the northern Mexican Car-
ibbean, as conceptualized by Chávez and Hidalgo (1988) and Chávez
et al., (2007). These would tend to have characteristics in common with
less developed ecosystems, such as the coastal lagoons of Table 5.
For ecosystems with low development, such as the Términos lagoon
(Table 5), during three annual periods, the highest DW was present at
the lower trophic levels, i.e. the control of the energy flow was bottom-
up (Abascal-Monroy et al., 2015) due to the large primary production
characteristic of this type of ecosystem (Lara-Domínguez et al., 2011).
In contrast, the reefs of the Caribbean Sea present a wasp-waist control,
with the exception of several reefs with high development, which
present a top-down control. The systems that generally exhibit a wasp-
waist control are those of upwelling regions, in which few species of
intermediate trophic level are vital for their large biomasses (e.g. an-
chovies, sardines). However, long-term fluctuations can alter the bal-
ance of the system by affecting its abundance and therefore alter the
food provision of those who prey on them (Cury et al., 2000). Despite
having detected a wasp-waist control in the reefs of the Mexican Car-
ibbean, this can favor their persistence and resilience, since the great
diversity of prey at the intermediate trophic level (with different life
histories, adaptations and ranges of tolerance to long-term fluctuations)
means that the food availability of predators is unaffected.
Hypothetically, if there are coral reefs with even lower stages of
development, such as those suggested by Chávez and Hidalgo (1988)
and Chávez et al., (2007), in the Gulf of Mexico (which have evolved in
eutrophic environments) (Salas-Pérez et al., 2015; Jordán-Garza et al.,
2017), then it is possible that their flow control would be bottom-up
(similar to that of coastal lagoons) (Abascal-Monroy et al., 2015) and
the energy recycling would be lower, as suggested by Ulanowicz
(1986). Under this argument, a gradient in flow control is perceived for
different stages of development, being bottom-up in immature ecosys-
tems, wasp-waist in ecosystems with intermediate development and
top-down in mature ecosystems. To determine if this hypothesis is true,
it is necessary to address reefs with different levels of geomorphological
development, under different physicochemical conditions and under
the same ecological construction scheme.
On the other hand, the number of connections and the degree of
intermediation was the same for the three development stages of the
studied reefs. Despite this, the higher trophic levels were notable for
presenting a greater number of connections and a position of great
importance in trophic intermediation. This is contrary to that reported
by Cruz-Escalona et al., (2016) in estuarine ecosystems with a low
development stage such as Bahía Magdalena where trophic groups with
a high Dc and Bc have intermediate trophic levels (Table 5). The
Magdalena Bay trend is consistent for other estuarine systems; hence
Scotti and Jordán (2010) suggested that greater emphasis should be
placed on intermediate positions in conservation policies rather than
final predators. However, the position and importance of the species
and/or trophic groups may depend on the development stage of an
ecosystem in such a way that the management policies must be directed
towards the particular characteristics of each ecosystem. For example,
in estuarine ecosystems it is important to protect intermediate trophic
levels, while in reefs, such as those of the Mexican Caribbean, efforts
should be focused on preventive actions of protection for species of
higher trophic levels.
Finally, bearing in mind the patterns obtained between topological
indices and development stages, their use in the detection of develop-
mental stages can be considered in conjunction with attributes pro-
posed by Odum (1969) and Ulanowicz (1986). Therefore, Dc and Bc
can be considered within the G1 attributes since they can indicate
broad scales, Cc in G2 since it differentiates three development stages

8
J. Argüelles-Jiménez, et al. Ecological Indicators 110 (2020) 105866

Table 6
Functional groups for each Mexican Caribbean coral reefs.
Functional groups PN PMo PMa Aku BP Yy PA PH Ta EP Ma Xa Xc

Large sharkslrays, carnivorous – – – – 1 – – – 1 – 1 – 1

Sharks/scombrids, carnivorous – – – – – 1 1 – – 1 1 – 1
Large jacks, carnivorous – – – – – – – – – 1 – – –
lntermediate jacks, carnivorous 1 1 1 1 1 1 1 1 1 1 1 1 1
lntermediate reef fish, carnivorous 1 1 1 1 1 1 1 1 1 1 1 1 1 1
Large-intermediate schooling fish, pelagic – – – – – – – – – – 1 – –
lntermediate reef fish, carnivorous 2 1 1 1 1 1 1 1 1 1 1 1 1 1
Kyphosidae, herbivorous – 1 1 1 1 1 1 1 1 1 1 1
lnterrnediate reef fish, herbivorous 1 1 1 1 1 1 1 1 1 1 1 1 1 1
lnterrnediate reef fish, herbivorous 2 – – – – – – – – – – 1 1 1
Large reef fish, carnivorous 1 1 1 1 1 1 1 1 1 1 1 1 1
Intermediate reef fish, carnivorous 3 1 1 1 1 1 1 1 1 1 1 1 1 1
Small reef fish, carnivorous 1 1 1 1 1 1 1 1 1 1 1 1 1 1
Small reef fish, carnivorous 2 1 1 1 1 1 1 1 1 1 1 1 1 1
Large groupers, carnivorous – – 1 1 1 1 – – 1 1 1 1
lntermediate reef fish, carnivorous 4 1 1 1 1 1 1 1 1 1 1 1 1 1
Small reef fish, omnivorous 1 1 1 1 1 1 1 1 1 1 1 1 1 1
Small reef fish, omnivorous 2 1 1 1 1 1 1 1 1 1 1 1 1 1
Small reef fish, omnivorous 3 – – – – 1 1 – – 1 – – – 1
Large Scaridae, herbivorous 1 – 1 1 1 1 1 – 1 1 1 1 1
lntermediate Scaridae, herbivorous 1 1 1 1 1 1 1 1 1 1 – – –
Small Scaridae, herbivorous 1 1 1 1 1 1 1 1 1 1 1 1 1
Blenniidae, herbivorous – – – – 1 1 – 1 1 – – – 1
Small Gobiidae, carnivorous – 1 1 1 – 1 1 1 1 1 1 1 1
Dolphins 1 1 1 1 1 1 1 1 1 1 1 1 1
Seabirds 1 1 1 1 1 1 1 1 1 1 1 1 1
Squids 1 1 1 1 1 1 1 1 1 1 1 1 1
Seaturtles 1 1 1 1 1 1 1 1 1 1 1 1 1
Octopuses 1 1 1 1 1 1 1 1 1 1 1 1 1
Lobsters 1 1 1 1 1 1 1 1 1 1 1 1 1
Crabs 1 1 1 1 1 1 1 1 1 1 1 1 1
Shrimp/Stomatopod 1 1 1 1 1 1 1 1 1 1 1 1 1
Small benthic arthropods 1 1 1 1 1 1 1 1 1 1 1 1 1
Asteroids 1 1 1 1 1 1 1 1 1 1 1 1 1
Echinoids 1 1 1 1 1 1 1 1 1 1 1 1 1
Grastropods 1 1 1 1 1 1 1 1 1 1 1 1 1
Chitons/Scaphopods 1 1 1 1 1 1 1 1 1 1 1 1 1
Polychaete/Priapuloid/Ophiuroids 1 1 1 1 1 1 1 1 1 1 1 1 1
Bivalves 1 1 1 1 1 1 1 1 1 1 1 1 1
Sponges 1 1 1 1 1 1 1 1 1 1 1 1 1
Corals/Sea anemones 1 1 1 1 1 1 1 1 1 1 1 1 1
Zooplankton 1 1 1 1 1 1 1 1 1 1 1 1 1
Decomp/Microfauna 1 1 1 1 1 1 1 1 1 1 1 1 1
Phytoplankton 1 1 1 1 1 1 1 1 1 1 1 1 1
Benthic producers 1 1 1 1 1 1 1 1 1 1 1 1 1
Detritus 1 1 1 1 1 1 1 1 1 1 1 1 1

The key to the reefs is shown in Fig. 1.

Table 7 Table 8
PREBAL analysis among the trophic level (TL) with three vital biological de- Marginal effects (Lambda) obtained from the forward selection summary and
scriptors: P/B, Q/B and B. inflation values (colinearity) obtained from the RDA.
Coral reef TL vs Log10 P/B TL vs Log10 Q/B TL vs Log10 B DA Lamda IF1 IF2 IF3

n r p-value n r p-value n r p-value A/CD 0.25 15.7 0 5.3

O/DC 0.25 0 0 0
PN 33 −0.46 ** 31 −0.35 * 36 −0.7 *** S 0.24 0 2.4 3.3
Pmo 33 −0.46 ** 31 −0.36 * 37 −0.71 *** TST* 0.24 98975.7 94420.6 –
Pma 34 −0.43 ** 33 −0.34 * 38 −0.69 *** NPP 0.24 0 0 8.9
Aku 36 −46 ** 33 −0.3 * 39 −0.7 *** A 0.24 0 94741.3 0
BP 38 −0.5 ** 36 −0.42 * 39 −69 *** O 0.24 97522.6 0 0
Yy 39 −0.49 ** 35 −0.4 * 42 −0.6 *** DC 0.24 0 0 0
PA 36 −0.48 ** 34 −0.4 * 39 −0.72 *** FCI*** 0.12 0 – –
PH 34 −0.52 ** 30 −0.41 * 35 −0.73 *** B/TST** 0.08 1795.7 – –
Ta 37 −0.47 ** 36 −0.38 * 41 −0.52 ** PP/B** 0.08 1499.3 – –
EP 38 −0.49 ** 36 −0.41 * 37 −0.6 *** PP/R** 0.04 29 – –
Ma 38 −0.53 ** 37 −0.44 ** 42 −0.69 ***
Xa 36 −0.45 ** 34 −0.37 * 39 −0.67 *** DA: development attributes, IF: Inflation factor and subscripts 1, 2, 3 correspond
Xc 40 −0.5 ** 38 −0.43 ** 43 −0.54 ** to the three RDA models made to obtain the lowest colinearity. *** Attribute
with little explanatory power and low colinearity discarded in the first model;
The key to the reefs is shown in Fig. 1. Significance of the p-value: * for ** Attributes with little explanatory power and high colinearity that were
p < 0.05, ** for p < 0.01 and *** for p < 0.0001. discarded in the first model (IF1); * Attribute that due to its high colinearity was
discarded in the second model (IF2).

9
J. Argüelles-Jiménez, et al.
described herein, and DW in G3, because it partially differentiates one
of the three scales.
5. Conclusions
The present study is perhaps the first one that seek and provide
evidence of the existence of a gradient of ecosystemic maturity linked to
the geomorphological and/or structural development of the reefs of the
Caribbean Sea through development attributes. In this way, we con-
cluded that as the geomorphological development of the reefs increases
towards the south of the Mexican Caribbean, so does their degree of
maturity.
The statistical analyzes used gave the guideline to identify three
groups of development attributes, which have been considered here as
G1, G2 and G3. Each one exhibits different information in relation to
ecosystem development stage, so depending on the objective of the
research it will be necessary to use one or all groups of attributes.
Topological indices helped to establish that the results obtained
through the topology of the trophic networks depend on the degree of
development of the reef ecosystems, likewise, it is proposed that the
topology of the system can be used as developmental attributes to es-
tablish development stages.
The determination of development stages of coral reefs can help to
formulate management plans and measures, so that more rational use of
resources can be made in coral reef ecosystems with different degrees of
maturity.
CRediT authorship contribution statement
Jimmy Argüelles-Jiménez: Conceptualization, Writing - review &
editing, Formal analysis, Writing - original draft. Jorge Christian Alva-
Basurto: Writing - review & editing, Data curation, Writing - original
draft. Horacio Pérez-España: Conceptualization, Writing - review &
editing, Writing - original draft. Manuel J. Zetina-Rejón: Writing -
review & editing, Formal analysis, Writing - original draft. Jesús
Ernesto Arias-González: Writing - review & editing, Data curation,
Writing - original draft.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
We want to thank Dr. Robert Ulanowicz, Dr. Fabian Rodríguez
Zaragoza and the reviewers for their accurate observations in the re-
view of this article as well as Centro de Investigación en Ciencias de
Información Geoespacial of CINVESTAV-Mérida for their support to run
trophic routines in their processors.
Funding
This study was supported by the Consejo Nacional de Ciencia y
Tecnología de México (CONACyT) and the Secretaria del Medio
Ambiente y Recursos Naturales (SEMARNAT) through the project
“Diversity and functioning of the Mexican Caribbean coral reefs”.
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