Open Journal of Marine Science, 2012, 2, 150-156
http://dx.doi.org/10.4236/ojms.2012.24018 Published Online October 2012 (http://www.SciRP.org/journal/ojms)
Changes in Mangrove Epifaunal Assemblages Caused by
Forest Logging during Hunting of the Neotropical
Cormorant (Phalacrocorax brasilianus) on the Colombian
Pacific Coast
Carlos Andrés Satizabal R.1, Jaime Ricardo Cantera Kintz1, Paula Cristina Sierra-Correa2
1Universidad del Valle, Ecology of Estuaries and Mangroves Research Group (ECOMANGLARES), Cali, Colombia
2Marine and Coastal Research Institute (INVEMAR), Cerro Punta Betín, Santa Marta, Colombia
Email: casatiza@gmail.com
Received May 8, 2012; revised July 6, 2012; accepted July 15, 2012
ABSTRACT
Although the importance of mangroves is clearly recognized around the world, these ecosystems are being strongly al-
tered by the logging of their forests for multiple purposes. The Colombian Pacific coast is not an exception to this situa-
tion, and apart from the traditional logging of wood, the hunting of the Neotropical Cormorant or Pato-cuervo (Pha-
lacrocorax brasilianus), an activity largely unknown but widespread in the region, is also causing the logging of great
extensions of mangroves. The aim of this research was to determine if the assemblages of mollusks and crustaceans of
these mangroves are being affected by the hunting of the cormorant. To answer this question, quantitative samplings
were realized in four transects in logged and unlogged mangrove areas on the southwestern coast of the Colombian Pa-
cific and diversity, equitability and dominance of macrofaunal assemblages of mangroves were calculated. The data
show that although significant differences between diversity indices were not found, there were important differences in
equitability (total J’: 0.55 in T1, 0.77 in T2, 0.46 in T3 and 0.65 in T4), specific dominance, and composition of spe-
cies (T1: 11 species, T2: 13, T3: 9 and T4: 11) between logged and unlogged areas. Based on these results, although
forest structure and interstitial salinity were different among transects, we conclude that the present practice of exploita-
tion of the Neotropical Cormorant is affecting the epifaunal populations of mangroves, causing changes in the composi-
tion and dominance of species.
Keywords: Mangrove; Mollusks; Crustaceans; Neotropical Cormorant; Colombian Pacific
1. Introduction
It is well known that mangrove forests are ecosystems of
great ecological and economic importance, since by their
nature they provide shelter, food, and protection for
many species, among which are fish, crustaceans, mol-
lusks, and many others [1-3]. The most important role of
mangroves is that of “nurseries” for the birth and deve-
lopment of early stages of these species, representing a
key role not only in the maintenance of mangroves, but
also in other ecosystems, both marine and freshwater [3].
Although the importance of mangrove ecosystems is well
recognized, these ecosystems are being severely altered
throughout the world, because of logging for multiple
purposes.
On the Colombian Pacific coast, although logging is
legally prohibited, large tracts of mangrove forest are
being cut, mainly for exploitation of timber resources,
but cutting also has been done historically for tannin ex-
traction, drying out mangroves for coconut crops, or es-
tablishment of ponds for shrimp farming. An apparently
new activity on a massive scale in the south of the coun-
try, about which there are few references, is the exploita-
tion of the Neotropical Cormorant or Duck-Crow (Pha-
lacrocorax brasilianus [Gmelin]), family Phalacrocora-
cidae, previously known as P. bougainvillii).
This species nests in the tops of mangrove trees, and
the adults and young (the latter in greater proportion) are
consumed locally by the surrounding human communi-
ties; this is causing cutting of large areas of forests to
obtain the animals. Populations of this species are af-
fected by both the loss of individuals by hunting and by
habitat destruction, resulting in decreased reproductive
success of these birds [4]. Although hunting is unprece-
dented anywhere else on the American Pacific coast,
some authors have pointed out the effect it could have on
*Corresponding author.
C
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C. A. SATIZABAL R. ET AL. 151
the mangrove ecosystem and on plant and animal com-
munities associated with that ecosystem [5].
The species composition of macrobenthic communities
associated with mangrove ecosystems is known from a
taxonomic and ecological viewpoint in some regions of
the Colombian Pacific coast for both mollusks [3,6-12]
and crustaceans [3,13,14]. Ecological studies of the com-
munities associated with mangroves are rare in the Pa-
cific Coast [3,15], and only a few studies examine the
community structure [9,16,17].
Mollusks and crustaceans are the most remarkable or-
ganisms of mangroves, for both species richness and the
abundance that some of them present. These two groups
live on both mangrove trees and in the substrate and are
known as an important part of the mangrove benthic
community; they are key links in food webs of the eco-
system [18,19]. Although most of these species are also
found on fallen logs or associated with the soil, it can be
seen that the cutting of mangroves for the exploitation of
Neotropical Cormorants may affect populations of these
two groups and epibenthic communities in general, as
has been recorded in other parts of the world [20].
The aim of this paper was to examine the impact of the
cutting of mangrove forests for Neotropical Cormorant
capture on the structure of the mangroves and on the
composition and abundance patterns of mangrove epi-
benthic organisms, including crustacean and mollusk
populations, on the Colombian Pacific coast.
2. Methods
2.1. Study Area
The study area was the municipality of Timbiquí, located
in southwestern Colombia on the Pacific coast, between
2˚42.213'N, 77˚46.398'W and 2˚56.515'N, 77˚39.253'W.
The average air temperature is 28˚C, mean annual rain-
fall is close to 6000 mm, and relative humidity is 93%.
The main rivers that supply the municipality are the
Timbiquí river, the Saija, and the Bubuey. These rivers
flow into the Pacific Ocean, forming wide river mouths
that have tidal deltas and accumulations of sediment in
coastal edges covered with mangrove vegetation. Man-
groves cover an area that reaches 8545 ha. The vegeta-
tion consists mainly of white mangrove (Laguncularia
racemosa), black or iguanero mangrove (Avicennia ger-
minans), piñuelo (Pelliciera rhizophorae), nato (Mora
oleifera), and red mangrove (Rhizophora mangle and
Rhizophora racemosa), as well as other target species.
Rhizophora species are the most dominant and fre-
quent individuals, with heights over 30 m [21].
Sampling was conducted under the project “Zoning
and Management of Mangroves in the Municipality of
Timbiquí”, agreement No.222, INVEMAR-MAVDT.
2.2. Sampling Areas
In order to see whether there were differences in the
composition and structure of epifaunal communities
among areas subjected to logging, areas in which Cor-
morant hunting has been carried out, areas with other
kinds of human interference, and areas without apparent
intervention, four areas were selected (Figure 1): the first
(Transect 1) is a mangrove area near agricultural activity
with a possible effect due to this activity, the second
(Transect 2) is non perturbed mangrove having higher
interstitial salinity, the third (Transect 3) is an area that
was recently logged to catch Neotropical Cormorants,
and the fourth (Transect 4) is an area with no apparent
intervention. This transect have similar salinity to tran-
sects 1 and 2 but corresponds to a well developed man-
grove forest without perturbation. Research was carried
out to study the characteristics of epibenthic assemblages
of organisms in relation to the structure of the mangrove
forest, to determine the effect that logging for hunting
Cormorant, has had on the stability of the epifaunistic
communities associated with mangroves.
2.3. Study of the Structure of the Mangrove
Forest
To determine the structure of the forest, the following
variables were measured for each tree in each transect,
using the point-quarter method: distance to the central
point (m), species, diameter (cm), height (m); from these
measurements density (No. of individuals/ha), basal area
(m2/ha), and total height were calculated. Structure index
are used to determinate the degree of perturbation of
mangrove forests.
2.4. Structure of Epibenthic Faunal Assemblages
Sampling the epifauna associated with mangrove forest
Figure 1. The study area showing the location of the four
sampling mangrove areas in Pacific coast of Colombia
(PCC), Tropical eastern Pacific.
Copyright © 2012 SciRes. OJMS
C. A. SATIZABAL R. ET AL.
Copyright © 2012 SciRes. OJMS
152
was done based on transects used for determining the
structure of the forest. From this line two transects were
located 10 m on either side of the line and parallel to it,
with a length of 50 m.
Along each transect, three quadrants of 2 × 3 m were
demarcated. In each of these, the number of species and
number of individuals found on both the substrate and on
the surface of the trees (branches, trunks and roots) were
recorded. The species were identified in situ when possi-
ble, or samples were taken and fixed in alcohol for
transport and laboratory identification.
With the data obtained, an analysis of similarity was
carried out between areas using the Bray-Curtis index
and represented in a dendrogram (cluster analysis) to
determine the similarities in species composition among
the four zones. Using the abundance and richness data,
Shannon-Wiener diversity index (H’), Pielou equitability
(J’) and Simpson dominance (D) were calculated using
the Biodiversity Pro software© Version 2.
The indices found were compared between the study
areas by a two-factor analysis of variance ANOVA (tran-
sect and quadrant) and a Duncan test to determine which
data sets were causing this difference. These tests were
conducted using SPSS© 15.0 software and STATIS-
TICA 7.0©.
3. Results
3.1. Structure of the Mangrove Forest
We found significant differences in the structural char-
acteristics of mangrove forests in the four zones (Table
1). Transect one (T1) presents data indicating that the
forest is in good condition but is still somewhat influ-
enced by the practice carried out in adjacent agricul-
tural areas. In transect two (T2) the forest has good
structural properties; this is the closest area to another
area logged for the capture of the Neotropical Cormo-
rant, so presumably this is the state of naturally occur-
ring forest that is used by the birds and later is logged.
In transect three (T3) trees appear very thin and
small, corresponding to an area that was logged re-
cently to catch Neotropical Cormorants, and which is
in process of regeneration. Transect four (T4) is an area
without intervention that has relatively tall trees, with
an average of 19 m, and its average density is charac-
teristic of well-developed forest. Structural index show
that the mangroves of Transects 1, 2 and 4.
3.2. Structure of Epibenthic Faunal Assemblages
A list of the species found and their abundances in each
transect is shown in Table 2. This table records two spe-
cies of the genus Anadara, because, although these spe-
cies are end of aunistic, they were found on the surface
of the substrate and therefore were included on the list.
Based on the results of richness and abundance taken in
the area, diversity, equitability and dominance indices
were determined for both mollusks and crustaceans to-
gether and for each group separately. The results are
shown in Table 3; the boxes marked with an asterisk (*)
correspond to areas where only one species was found.
Transect with the highest richness is T2 and the highest
abundance is T4. T3 has a high number of individuals,
but the 49% is of one species. Dominance was the high-
est in T3 (0.336) and lowest in T2 (0.123).
The mollusks showed the highest similarity between
T4 and T2 (80%) (Figure 2(a)), while crustaceans had
greater similarity between T4 and T1 (85.7%) (Figure
2(b)). When data for the two groups were combined, they
showed a grouping similar to that of crustaceans, also
showing an association of T1 with T4 (73.7%) and T3
with T2 (78.3%), as seen in Figure 2(c).
The results of the ANOVA can be seen in Table 4.
The only significant difference between the studied tran-
sects occurred in the diversity index (H) for mollusks,
and the equitability index (J) for mollusks and crusta-
ceans together.
The results of Duncan’s test for equitability of the epi-
fauna can be seen in Table 5, where boxes marked (*)
show a significant difference. T3 transect data are nota-
bly different with the other areas, especially in the last
quadrant (3.3 {6}), which corresponds to the more inter-
nal area of logged forest for the exploitation of the
Neotropical Cormorant. The data in this quadrant show
significant differences from many of the data in the other
transects.
Table 1. Structural characteristics of the mangrove forest and interstitial salinity for each studied transect in mangrove area
of Timbiqui (PCC).
Mean high (m) Salinity (ups)
Transect Density (Ind/ha) Seedlings Saplings Taper High max. (m)Basal area (m2/ha) Outside Inside
1 1474 6.0 8.0 16.0 25 45 9.4 8.6
2 2090 6.0 10.0 17.0 35 119 18.3 14.8
3 776 5.0 9.0 13.0 17 11 6.8 4.9
4 642 5.0 8.0 19.0 25 20 7.6 4.2
C. A. SATIZABAL R. ET AL. 153
Table 2. Species of mollusks and cr ustaceans and their abundance s found in four transects in the mangrove zone of Timbiquí
(PCC).
Groups Family Species T1 T2 T3 T4
Anadara tuberculosa 1 5 0 3
Arcidae Anadara similis 0 0 0 1
Littoraria zebra 1 1 6 39
Littoraria fasciata 6 1 0 36
Littorinidae
Littorina scabra 1 0 0 0
Cerithidea mazatlanica 16 2 52 32
Potamididae Cerithidea pulchra 1 5 2 0
Teredinidae Teredo sp. 0 0 100 0
Mollusks
Muricidae Thais kiosquiformis 1 0 35 95
Goniopsis pulchra 7 7 2 3
Aratus pisonii 0 5 0 2
Grapsidae
Pachigrapsus tranversus 6 2 4 3
Gercarcinidae Gecarcinus sp. 0 2 0 0
Uca sp.1 1 11 2 1
Ocypodidae Uca sp.2 0 6 1 1
Chthamalidae Chthamalus panamensis 0 1 0 0
Xanthidae Eurypanopeus transversus 1 1 0 0
Crustaceans
Total 42 49 204 216
Table 3. Indices of diversity (H'), equitability (J'), and dominance (D) for each quadrant and total per transect of epibenthic
fauna of a mangrove area of Timbiquí (PCC).
Index
Line quadrant Repetition H' J' D
4 1 1 0.367 0.472 0.574
4 1 2 0.528 0.625 0.382
4 2 1 0.687 0.882 0.192
4 2 2 0.627 0.805 0.271
4 3 1 0.567 0.942 0.231
4 3 2 0.540 0.898 0.304
T4 -- -- 1.548 0.645 0.276
3 1 1 0.815 0.782 0.228
3 1 2 0.441 0.567 0.471
3 2 1 0.476 0.681 0.424
3 2 2 0.618 0.795 0.292
3 3 1 0.196 0.252 0.802
3 3 2 0.354 0.589 0.543
T3 -- -- 1.025 0.467 0.336
2 1 1 0.450 0.747 0.373
2 1 2 0.647 0.831 0.220
2 2 1 0.460 0.764 0.399
2 2 2 0.673 0.963 0.095
2 3 1 0.636 0.910 0.167
2 3 2 0.297 0.985 0.429
T2 -- -- 1.851 0.722 0.124
1 1 1 0.415 0.870 0.333
1 1 2 0.697 0.896 0.167
1 2 1 0.308 0.511 0.637
1 2 2 0.391 0.819 0.393
1 3 1 0.437 0.726 0.434
1* 3 2
T1 -- -- 1.326 0.553 0.217
*Zone in which only one species was found.
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C. A. SATIZABAL R. ET AL.
Copyright © 2012 SciRes. OJMS
154
Table 4. ANOVA, two factors (α = 0.05) (H' = epifaunal diversity, J' = epifaunal equitability, D = epifaunal dominance).
deg. of freedom SS MS F p
TRANSECT 3 0.111191 0.037064 1.2859 0.323812
QUADRANT 2 0.135944 0.067972 2.3583 0.136834
Transect*Quadrant 6 0.171889 0.028648 0.9940 0.471531
H'
Error 12 0.345868 0.028822
TRANSECT 3 0.21338 0.07113 3.9981 0.034636*
QUADRANT 2 0.01891 0.00945 0.5314 0.600998
Transect*Quadrant 6 0.33116 0.05519 3.1025 0.045013*
J'
Error 12 0.21348 0.01779
TRANSECT 3 0.191070 0.063690 1.9499 0.175464
QUADRANT 2 0.117047 0.058523 1.7917 0.208496
Transect*Quadrant 6 0.312188 0.052031 1.5930 0.231674
D
Error 12 0.391953 0.032663
Table 5. Duncan test for equitability of the epifaunistic community (J’). Interaction 1 × 2 (1-Transect, 2-Quadrant).
{1} {2} {3} {4} {5} {6} {7} {8} {9} {10} {11} {12}
4 1 {1} 0.069 0.030* 0.387 0.2120.356 0.125 0.057 0.022* 0.046* 0.4000.056
4 2 {2} 0.069 0.609 0.263 0.4670.015*0.690 0.889 0.491 0.789 0.2450.886
4 3 {3} 0.030* 0.609 0.125 0.2420.007*0.389 0.694 0.840 0.786 0.1140.699
3 1 {4} 0.387 0.263 0.125 0.6430.102 0.430 0.223 0.093 0.184 0.9440.221
3 2 {5} 0.212 0.467 0.242 0.643 0.050 0.709 0.406 0.184 0.343 0.6120.402
3 3 {6} 0.356 0.015* 0.007* 0.102 0.050 0.028*0.012*0.005* 0.010* 0.1060.012*
2 1 {7} 0.125 0.690 0.389 0.430 0.7090.028* 0.614 0.304 0.531 0.4060.608
2 2 {8} 0.057 0.889 0.694 0.223 0.4060.012*0.614 0.570 0.886 0.2050.997
2 3 {9} 0.022* 0.491 0.840 0.093 0.1840.005*0.304 0.570 0.654 0.0840.572
1 1 {10} 0.046* 0.789 0.786 0.184 0.3430.010*0.531 0.886 0.654 0.1680.889
1 2 {11} 0.400 0.245 0.114 0.944 0.6120.106 0.406 0.205 0.084 0.168 0.204
1 3 {12} 0.056 0.886 0.699 0.221 0.4020.012*0.608 0.997 0.572 0.889 0.204
4. Discussion
The results of the study showed that the logging of man-
groves to capture Neotropical Cormorants affects the size
and development of mangroves and, in consequence, the
composition, species dominance, and equitability of epi-
benthic communities, although the diversity indices show
small differences. Although pacific Colombian man-
groves have relatively low diversity and richness, all
studied index had lower values in T3 (where is the im-
pact of the mangrove logging to capture cormorant nest-
lings) than the other three transects. In terms of species
composition, diversity and evenness the groups formed
indicate differences between Transects with high (T3)
and low (T1, T2 and T4) perturbation due to the capture
of the cormorant; although some areas had different stru-
ctural characteristics at the time of the study (T1 man-
groves slightly affected, T2 non perturbed mangroves but
geographically close to an area with strong perturbations
and T4 unaffected mangroves). These places are similar
estuarine mangrove areas, which means that they possi-
bly had a similar species composition. This is particularly
notably in the areas where transects two (T2) and three
(T3) were located, which served as nesting sites for
Neotropical Cormorants; however, T3 suffered exploita-
tion of the bird and has a forest with completely different
characteristics, with a structure that indicates a low level
of development, in a state of regeneration. The differ-
ences in species composition of epifauna in these areas
are due to changes in the structural characteristics of the
forest, which have led to the emergence of species that
are able to rapidly colonize these environments; these
species are found naturally in any ecosystem that has
been altered repeatedly or at such a high level as pre-
sented in this area [22]. In the mangroves studied, the
remains of trees left on the substrate as a result of log-
ging have resulted in the proliferation and abundance of
two species: Thais kiosquiformis and Teredo sp., which
C. A. SATIZABAL R. ET AL. 155
(a)
(b)
(c)
Figure 2. Cluster analysis by transect for epibenthic fauna
of mangroves in Timbiquí (PCC). (a) Mollusks; (b) Crus-
taceans; (c) Mollusks and crustaceans combined.
are found in decaying logs, which provide shelter and
defense against desiccation [23,24]. Both are species that
live in other mangroves when there are many dead trunks.
The abundance of these species in T3 (where logging has
occurred) is the main factor that modifies the structure of
assemblages of mangrove epifauna. Crustacean species
such as Pachygrapsus transversus and Goniopsis pulchra,
can support large changes in habitat conditions [25,26]
and therefore can inhabit in all mangrove areas. Unlike,
some littorinids and Aratus pisonii are not present in
perturbed mangrove.
This is why the differences in diversity are small,
which is different than expected for the different areas.
However, this is not surprising; because these indices
take into account both abundance and species richness,
resulting in the modification of both at different levels
without altering the value of the index.
The results found in this research coincide with the
models presented in other works [22], which indicated
that the effects on diversity of a disturbance such as in-
tensive logging of mangroves for capturing Neotropical
Cormorants are real. Changes do occur in species rich-
ness and abundance of individuals, reflected in the do-
minance and equitability of the species, more than in the
diversity index. The decrease in the number of individu-
als of different species has been found in other studies
([20,27]), which examined the effect of various types of
disturbance on mangrove forests, including logging for
other purposes different to capture birds.
5. Conclusion
It can be concluded that the exploitation of Neotropical
Cormorants by the current practice of logging the forest,
in addition to causing significant alterations in the struc-
ture of mangroves, also affects the structure of assem-
blages of epifaunistic mollusks and crustaceans that in-
habit them. These changes are manifested mainly in the
composition, dominance, and equitability of the species,
and slightly in species diversity, where the physical and
chemical changes in the ecosystem caused by vegetation
change, salinity among others, cause the disappearance-
appearance and/or proliferation of a few species that are
favored by the new features of the habitat. These changes
could have a significant economic impact on the inhabi-
tants of the Pacific coast, given its dependence to a large
extent on the resources provided by the mangrove eco-
system. This study is an input to management of this
mangrove ecosystem and its associated avifauna.
6. Acknowledgements
The authors express their gratitude to the Institute of Ma-
rine and Coastal Research—INVEMAR, through which
this work was developed in the framework of the project
“zoning and management of mangroves in the munici-
pality of Timbiquí”, agreement No. 222 INVEMAR-
MAVDT, and all people linked to this project, who con-
tributed significantly: A. Sanchez, C. Muñoz, F. Bedoya,
A. Moreno. We also thank the Research Group in Estu-
aries and Mangroves (ECOMANGLARES), and its
members J. F. Lazarus, A. M. Cobo, L. A. Lopez de
Mesa, E. Londoño, L. Herrera and M. A. Ocampo for
their support in identifying individuals and statistical
analysis. We are grateful to the professor Philip A.
Silverstone-Sopkin of the Universidad del Valle for cor-
recting the English grammar.
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