Changes in Mangrove Epifaunal Assemblages Caused by Forest Logging during Hunting of the Neotropical Cormorant (<i>Phalacrocorax brasilianus</i>) on the Colombian Pacific Coast

doi:10.4236/ojms.2012.24018

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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: [email protected]

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. 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.

C. A. SATIZABAL R. ET AL.

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.

C. A. SATIZABAL R. ET AL.

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

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*

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

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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