Vilardy&Polania 2002.Mollusc Fauna of Root-fouling Community, Archipiélago San Andrés&Old Provide

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Wetlands Ecology and Management 10: 273–282, 2002.

© 2002 Kluwer Academic Publishers. Printed in the Netherlands. 273

Mollusc fauna of the mangrove root-fouling community at the ColombianArchipelago of San Andres and Old Providence

Sandra Vilardy & Jaime PolanıaUniversidad Nacional de Colombia Sede San Andr´ es, Carretera Circunvalar de San Luis, Sector Free Town

#52-44, San Andr´ es Isla, Colombia, Tel: (+57) 8 5133310, Fax (+57) 8 5133390, E-mail: [email protected],

[email protected]

Key words: associated fauna, mangrove, molluscs, Mytilopsis sallei, Western Caribbean

Abstract

This paper advances a qualitative and quantitative preliminary characterization of the mollusc fauna associated

with the submerged roots of Rhizophora mangle L. in three mangrove areas with different degrees of anthropogenic

impact in the San Andrés (Hooker and Honda Bays) and Providence (Old Providence McBean Lagoon National

Park) archipelago in the Western Caribbean. The study was carried out during the dry and rainy seasons (July

and November, respectively) back in 1998. Samples were taken from 34 submerged roots which were not fixed

to the substrate. Several physico-chemical parameters were also measured in situ. All molluscs were identified

and counted and indexes of species richness, diversity, uniformity, similarity, dominance of species and density of

individuals were calculated. All in all 5,771 individuals belonging to 21 species of 17 families were counted. Most

of the species were epibenthic, herbivorous and with undifferentiated planctonic larvae, but most of the individuals

were epifaunal and attached as well as filter-feeders with planctonic larvae. Most individuals were found in juvenile

stages. The three sites, under different degrees of anthropogenic impacts, showed related values of species richness,

diversity and abundance, as well as densities of mollusc taxa in oceanic communities associated with mangrove

roots. Further research should be done to find similar responses in accompanying significant groups, such as

Crustacea and Polychaeta.

Introduction

Mangroves are considered one of the most product-

ive ecosystems within the tropics and the subtropics,

with distinctive faunal associations. Characteristically,

in mangroves the detritivores and consumers of high

trophic level are strongly integrated (Jiang and Li,

1995).

According to recent estimations, the Colombian

Caribbean has 135,398 hectares (ha) covered with

mangrove forests (Sanchez-Paez et al., 1997). In theSan Andrés island, the mangrove forests amount to

132 ha. Garcia and Gaviria (1996) and Sanchez-Paez

et al. (1997) have documented for the islands the death

of some mangroves due to mounting contamination.

This, in turn, can be either produced by human inter-

vention or by various physical and chemical factors

exerting long lasting impacts over the ecosystems spe-

cies’ composition and their structural relationships

(Diaz, 1995). Among the former sources of contam-

ination, petrogenic-generated hydrocarbons have been

detected in coastal sediments as well as in several

commercial fish species, in concentrations exceed-

ing those accepted by UNESCO. Some other anthro-

pogenic damage to San Andrés coastal ecosystems

include the destruction of plant formations, sewage,

dredging and landfill operations near the North End

between 1966 and 1970.

The fauna associated with mangrove roots havebeen studied all around the Caribbean. Perry (1988) in

Costa Rica, and Ellison and Farnsworth (1990, 1992)

and Ellison, Farnsworth and Twilley (1996) in Belize

have studied the interactions between mangrove roots’

productivity and growth and different organisms. Es-

pinoza (1978), Cruz-Abrego et al. (1994a, 1994b) and



274

Hernandez-Alcantara and Solis-Weiss (1995), have

studied the communities of the Terminos Lagoon and

the Contoy Island in Mexico, where they tried to es-

tablish some relationships between those communities

and the benthic species, making ecological annota-

tions of these species. Lalana and Perez (1985), and

Lalana et al. (1985) described the mangrove-roots’associated fauna in estuaries and sea related sites of

Cuba; while Cruz and Jimenez (1994) undertook the

listing of molluscs associated with mangrove areas

on the Pacific coast of Central America. Earlier on,

Batista (1980) had described the epibenthic com-

munities of Panama, while Keller and Jackson (1991),

Garrity and Levings (1993), and Levings and Garrity

(1994) assessed the effects of an oil spill on man-

grove areas on the Panamanian Caribbean coast in

April 1986. Sutherland (1980) described the fauna as-

sociated with the mangrove roots on the Venezuelan

coasts, and Orihuela et al. (1992) examined mass mor-

tality of the epibiota of mangrove roots in the highly

salinized lagoons of Venezuela. Diaz et al. (1992)

carried out a detailed analysis of different sampling

methods used to analyze those communities.

In Colombia several lists of species present along

the Caribbean coast were completed, particularly for

the Cartagena Bay and the Cienaga de los Vasquez

swamp (Perdomo, 1971; Perez and Victoria, 1977;

Cifuentes, 1980); the Cienaga Grande de Santa Marta

coastal lagoon (Palacio, 1978), the Tayrona National

Natural Park (Reyes, 1991) and the Old Providence

island (Skinner, 1994).

Other ecological assessments dealing with the dis-tribution of molluscs species (Contreras and Cantera,

1976, Cantera et al., 1983; Escallon and Cantera,

1989) and their natural history in the Colombian Pa-

cific coast (Cantera, 1978) have also been carried

out.

This paper characterizes the molluscs of the

mangrove-root fouling community, and presents some

ecological annotations of the species in three sites with

different levels of anthropogenic stress around the two

main islands of the Colombian Western Caribbean Ar-

chipelago of San Andrés, Old Providence and Saint

Kathleena. The research was carried out during two

successive climatic seasons: the dry and wet periods

of July and November, respectively.

Methods

The areas, at the San Andrés, Old Providence and

Saint Kathleena Archipelago (between 12◦–16◦ N,

and 78◦–82◦ W), located 800 km northwest of the

Colombian coastline, were selected in mangrove eco-

systems on the two former islands, where the tidalregime is narrow (40 cm). The weather is tropical

humid-dry, dominated by trade winds, with a dry

season between January and April and a rainy sea-

son starting early in May and picking up through out

November; and the mean temperature is 27.4◦C with

slight variations throughout the year (Diaz et al., 1995;

Angel, 1998).

Honda and Hooker Bays in San Andrés are located

on the north-east coast. Honda Bay has 34.4 ha riv-

erine mangrove at its north end and extends well into

the adjacent Hooker Bay (Figure 1) (Angel, 1998). In

Honda Bay, seagrasses and macroalgae share the same

space, and is considered as partially stressed. Hooker

Bay, in turn, has a 15.1 ha Rhizophora mangle fringe

mangrove. Among other stresses, the ecosystem has

undergone a chronic accumulation of hydrocarbons in

the sediments (Garcia and Gaviria, 1996). The Old

Providence McBean Lagoon, located in the east sector

of the island, possesses a large fringe mangrove, with

ca. 27 ha located behind the barrier reef, and can be

regarded as free of direct human impact.

Two samplings were carried out in each one of

these three areas. The first one in July 1998 (which

this research assumes as the end of the dry season)

and the second in November 1998 (rainy season). Thetwo samplings across Honda and Hooker Bays com-

prised a single root at each of 5 points along spatial

gradients in each case. In McBean Lagoon 7 roots

were sampled during the two periods. The parameters

measured in situ for each of the sampling sites were:

salinity, temperature and dissolved oxygen. The con-

centration of total aromatic hydrocarbons in sediments

was measured in the July’s sampling.

The sampling entailed the following procedure:

each root (submerged but not anchored) was covered

with a plastic bag to avoid losses of mobile species.

The roots were then cut loose above the high tidelevel. Water in the plastic bag was removed, and

every bag was then labeled, sealed and taken to the

laboratory of the National University of Colombia

at San Andrés, where they were refrigerated. In the

laboratory, the roots were measured and the associ-

ated molluscan individuals were separated manually,

preserved in neutralized 40% formalin and later con-



275

Figure 1. The San Andres, Old Providence and Saint Kathleena Archipelago. Location of sampling stations in Hooker Bay and Honda Bay

(San Andres Island) and Old Providence McBean Lagoon National Park (Old Providence Island).



276

served in 70% ethanol. The species were identified

and ecological annotations were made based on Keen

(1961), Warmke and Abbott (1962), Marcus and Mar-

cus (1963), Hadfield et al. (1972), Moore (1972), Ab-

bott (1974), Marcus and Hughes (1974), Rios (1985),

Clark (1994), Diaz and Puyana (1994), Cruz-Abrego

et al. (1994), Mikkelsen et al. (1995) and Calvo etal. (1998). Starting with the number of individuals for

each species, quantitative and qualitative descriptions

of species and communities were undertaken. The pro-

cedure ended up with a comparative analysis of the

studied areas using parameters such as density (indi-

viduals per root), species richness, Shannon-Weaver

diversity index, uniformity, species dominance and

Bray-Curtis similarity index.

Results

Physico-chemical factors

As shown in Table 1, the largest temperature fluc-

tuations were recorded in Hooker Bay, while Honda

Bay and the McBean Lagoon produced intermediate

and lower values, respectively. Salinity measurements

showed higher values and smaller variations in the

McBean Lagoon, while in Hooker Bay the salinity

values were the lowest of the three sites although it

had the widest variations. Salinity was higher in July

in the McBean Lagoon, despite the freshwater in-

put. Roots analysis: 34 submerged R. mangle roots

were examined, with a total surface of 2.38 m2; fromwhich 1.31 m2 were surveyed in July (Table 2). Three

roots of Honda Bay lacking individuals in November

remained uncounted.

Associated community

All in all 5,771 individuals of molluscs were found,

1,433 in July and 4,338 in November (Table 3).

Hooker Bay, Honda Bay and the McBean Lagoon had,

respectively, 5,408, 248 and 115 individuals belong-

ing to 21 species (2 were identified only to genus)

from 17 families, 7 orders and 2 classes. At specieslevel, 18.2% were Bivalvia and 81.8% Gastropoda.

At individual level, 94.3% were Bivalvia, 4.5% were

Prosobranchia and 1.3% were Opistobranchia. Out of

the 21 taxa of molluscs found at the Archipelago, 19

were identified to the species level, while two were

identified only to the genus level and 1 was recognized

as morphotype. From them, the following were newly

recorded for San Andrés: Caecum nitidum, Cerith-

ium lutosum, Elysia crispata, Haminoea antillarum,

H. succinea, Mytilopsis sallei, Pilbryspina leucocyma

and Zebina browniana.

Usually, some species prefer filamentous algal

mats, although no stratification along the root can be

recognized. Mytilopsis sallei populations at HookerBay were also found on the lower-internal parts of

the branching roots. The recorded species belong to

5 life forms according to their ground preferences:

vagile, epifaunal, semi-infaunal, sessile (attached),

and infaunal. At species level 47.6% were epifaunal,

23.8% sessile, 14.3% semi-infaunal, 9.5% infaunal,

and 4.8% vagile. At the individual level, 97.2% were

filter feeders, 1.0% carnivores, 1.0% herbivores, and

0.2% omnivores.

The molluscs found showed distinctive develop-

ment types: 57.1% had planctonic larvae, 14.3%

had direct development. The development type of

the remaining 6 species (28.6%) could not be es-

tablished. For 7 species all individuals were ma-

ture: Caecum nitidum, Cerithidium lutosum, Elysia

crispata, Littorina angulifera, Neritina virginea, Pil-

bryspira leucocyma and Zebina browniana. The in-

dividuals of 10 species were exclusively juvenile:

Bulla striata, Cerithium eburneum, Conus sp., Cyma-

tium pileare, Haminoea antillarum, H. succinea,

Isognomon bicolor, I. radiatus, Modulus modulus and

Serpulorbis sp.

Community characteristics

Altogether, the MacBean Lagoon survey showed the

highest values for species richness amounting to 18.

This was followed by Honda Bay (10) and Hooker

Bay (2). For both seasons 13 species were common,

5 were exclusive in July and 3 in November. The

largest diversity of species (Shannon-Wiener index),

were calculated for the MacBean Lagoon in both sea-

sons, while in Hooker Bay such diversity was lower

(Figure 2).

A classification carried out using the Bray-Curtis

similarity index showed 10 groups within the stations,

given by the presence and abundance of common spe-cies (Figure 3). Groupings according to season could

not be properly differentiated. Some of the groups

match a single root with a single species not found

elsewhere (root Jul. 1 MacBean Lagoon: E. crispata;

Jul. 3 McBean Lagoon 5 species and the only indi-

vidual found of P. leucocyma. On Nov. 1 Honda Bay:

the only 5 individuals of H. succinea found were coun-



277

Table 1. Temperature, salinity, concentration of aromatic hydrocarbons and dissolved oxygen in the

water column in Old Providence McBean Lagoon, and Honda and Hooker Bays, San Andres island,

in July and November 1998.

Site Date Temperature Salinity Aromatic Diss. Oxygen

(◦C) () hydrocarbons (µg g−1) (mg O2 l−1)

McBean 1 July 31.00 35.00 0.77 8.20

2 July 31.00 34.00 0.09 8.10

3 July 31.00 33.00 nd 6.80

4 July 30.00 35.00 3.54 6.50

5 July 20.00 35.00 0.13 7.90

6 July 29.00 36.00 0.83 7.50

7 July 29.00 38.00 0.86 7.20

McBean 1 Nov 30.00 28.00 nd 8.70

2 Nov 29.00 34.00 nd nd

3 Nov 29.00 35.00 nd nd

4 Nov 29.00 35.00 nd nd

5 Nov 28.50 35.00 nd 4.50

6 Nov 28.50 35.00 nd 6.60

7 Nov 28.00 25.00 nd 7.00

Honda Bay 1 July 27.00 32.00 0.86 5.80

2 July 27.00 31.10 0.64 6.50

3 July 26.50 35.00 1.43 6.30

4 July 26.00 35.00 1.45 5.70

5 July 26.00 35.00 1.10 5.30

1 Nov 28.00 36.00 nd 5.60

2 Nov 28.00 32.00 nd 5.30

3 Nov 28.90 30.00 nd 6.00

4 Nov 29.20 36.00 nd 7.70

5 Nov 29.00 36.00 nd 8.00

Hooker Bay 1 July 28.00 8.00 0.00 3.30

2 July 27.50 6.00 0.05 3.80

3 July 26.00 8.00 0.32 4.80

4 July 27.00 15.00 0.46 5.30

5 July 28.60 19.00 0.49 3.70

1 Nov 30.00 26.50 nd 12.50

2 Nov 29.00 28.00 nd 9.60

3 Nov 28.80 24.00 nd 11.80

4 Nov 29.00 24.00 nd nd

5 Nov 29.00 26.00 nd nd

Table 2. Surface of Rhizophora mangle roots, number of individuals and species

of molluscs calculated for Old Providence McBean Lagoon, Honda Bay and

Hooker Bay San Andres Island in July and November 1998.

Hooker Bay Honda Bay McBean Lagoon Total

Surface (m2) 0.6873 0.6941 0.9985 2.3799

N. individuals 5,408 248 115 5,771

N. species 2 10 18 21



278

Figure 2. Richness, diversity and uniformity indexes of mollusc species of the mangrove-root fouling community in Old Providence McBean

Lagoon, Honda and Hooker Bays, San Andres island, in July and November 1998.



279

Table 3. Mean size (in mm), life stage (Juv.: juvenile; Adl.: adult; J-A: juvenile as well as adult), life form (Inf.: infaunal; Epi.:

epifaunal; EpA.: epifaunal attached; Vag.: vagil; Sem.: semi-infaunal), trophic habits (T. habits; Car.: carnivores; Her.: herbivores;

Dep.: deposits collectors; Omn.: omnivores; Fil.: filter feeders; HeD: herbivores and deposit collectors; OmD: omnivores and

deposit collectors; Unk.: unknown); type of development (T. dev.; PlL.: planctonic larvae; Dir.: direct development; PtL: planc-

totrophic larvae; Unk.: unknown), and abundance (in number of individuals) of mollusc species of the mangrove-root fouling

communities in Old Providence McBean Lagoon and Hooker and Honda Bays in San Andres island, Colombian Caribbean, in

July and November 1998.

Taxa Mean Life Life T. T. Hooker Bay Honda Bay McBean Lagoonsize stage form habits dev. July Nov. July Nov. July Nov.

Bulla striata 5.5 Juv. Inf. Car. PlL. 0 0 6 9 21 8

Caecum nitidum 2.3 Adl. Epi. HeD. PlL. 0 0 0 28 0 0

Cerithidea pliculosa 14.0 J-A Epi. Unk. Unk. 0 0 0 0 11 0

Cerithium eburneum 9.0 Juv. Sem. Dep. Unk. 0 0 0 4 1 0

C. lutosum 15.0 Adl. Epi. OmD. Dir. 0 0 0 0 3 4

Columbella mercatoria 11.3 J-A Epi. Her. Unk. 0 0 0 0 6 0

Conus sp. 1.6 Juv. Sem. Car. Dir. 0 0 0 3 2 0

Cymatium pileare 10.4 Juv. Epi. Car. PlL. 0 0 1 4 2 0

Elysia crispata 36.0 Adl. Vag. Her. PtL. 0 0 0 0 1 0

Haminoea antillarum 3.0 Juv. Sem. Car. PlL. 0 0 0 3 3 0

H. succinea 2.2 Juv. Inf. Car. PlL. 0 0 0 12 1 9

Isognomon alatus 23.2 J-A EpA. Fil. PlL. 1 0 0 0 2 4

I. bicolor 3.9 Juv. EpA. Fil. PlL. 0 0 0 0 21 1

I. radiatus 8.3 Juv. EpA. Fil. PlL. 0 0 0 0 1 1

Littorina angulifera 16.0 Adl. Epi. Her. PlL. 0 0 1 0 1 0

Modulus modulus 5.0 Juv. Epi. Her. Dir. 0 0 0 0 2 1

Mytilopsis sallei 12.1 J-A EpA. Fil. PtL. 1,360 4,047 0 0 1 0

Neritina virginea 9.0 Adl. Epi. Her. Unk. 0 0 0 0 5 2

Pilbryspira leucocyma 8.6 Adl. Epi. Car. Unk. 0 0 0 0 1 0

Serpulorbis sp. 1.3 Juv. EpA. Fil. PlL. 0 0 0 173 0 0

Zebina browniana 3.5 Adl. Epi. Dep. Unk. 0 0 0 4 0 0

TOTAL 1,361 4,047 8 240 85 30

N. species 2 1 3 9 18 8

ted). Three of the groups have single root from the

McBean Lagoon; a fourth group comprised Honda

Bay roots and two more were formed by roots from

both sites.

Discussion

Characteristics such as the almost total dominance

of M. sallei and the huge abundance of individualsidentify the mollusc community associated with the

submerged roots of R. mangle at the Hooker Bay

site, with slightly more individuals found in Novem-

ber than in July. The environmental framework in

Hooker Bay restricts the mollusc community and its

vigor. Wide fluctuations of dissolved oxygen and sa-

linity, pollution by hydrocarbons and impacts gen-

erated by human activities could be the main stress

factors (Ellison and Farnsworth, 1992).

Diversity is reduced either by species death or by

the decline of secondary ground or by both (Levings

and Garrity, 1994) as observed in the Panamanian

communities largely affected by oil spills: species

such as Crassostrea rhizophorae and M. sallei were

the only molluscs remaining in the area after the

spills (Keller and Jackson, 1991). At the East In-

dian coast port of Visakhapatnam, M. sallei success-fully re-colonized the area affected by the presence

of hydrocarbons. Moreover, M. sallei can in fact bio-

accumulate and even magnify some pollutants in its

tissues (Mohan and Prakash, 1998).

Large colonies of Serpulorbis sp. and individuals

of C. nitidum were also typical at Honda Bay. Bulla



280

Figure 3. Bray-Curtis similarity cluster within July and November sampling stations in Hooker Bay and Honda Bay (San Andr es Island) and

McBean Lagoon (Old Providence Island) in the two sampling periods.

striata and C. pileare were common to both samplings.

At the Honda Bay and McBean Lagoon sites, the

physical environment, less altered than in Hooker

Bay, seems to favor the establishment of species-rich

mollusc communities. For instance, Honda Bay and

McBean Lagoon sites showed dramatic changes in the

species distribution from one root to another.

The community of the McBean Lagoon showed

a few individuals, and the species found had an het-erogeneous distribution over the roots. Bulla striata,

C. lutosum, H. succinea, I. alatus, I. bicolor, I. radi-

atus, M. modulus, and N. virginea represented 44.4%

of the species and remained in both seasons. High di-

versities at the McBean Lagoon reveal maximal use of

space by the species suggesting stronger interactions

between species and their environment, higher struc-

tural complexity, and higher availability of habitats

(Reyes, 1991).

Diversity of the mollusc communities associated

with the red mangrove roots is high, and the species

richness increases with low variations of salinity and

dissolved oxygen. The population structure may also

respond to short term variations and throughout dif-

ferent areas (e.g. very wide values recorded of variousindexes related to the studied sites and seasons. See

Bingham, 1992; Farnsworth and Ellison, 1996).

The mangrove roots environment is inherently het-

erogeneous and the communities grow over the roots

with no apparent patterns. Instead, these communit-

ies may form patches of single species on single



281

roots while, at the same time, they are absent in the

surrounding roots ( Z. browniana, C. mercatoria, C.

pliculosa and aggregations of Isognomon spp.). On the

other hand, each species may show its own vertical

distribution as a result of long term evolution strategies

(Jiang and Li, 1995).

It should be stated that young communities havea distinctive dynamic: larvae’s settling and mortal-

ity depend on predation and environmental factors

which, in turn, affect the distribution and compos-

ition of mature communities (Osman et al., 1992).

Mollusc diversity is determined by the availability of

microhabitats providing shelter and feeding grounds.

The roots lacked mobile individuals because they did

not have shelter or habitat potential. Naked roots re-

main, most of the time, free of mobile individuals,

although they may become optimal ground for lar-

vae and lead to the colonization and establishment of

attached communities (Wahl, 1989).

Filamentous algae are appropriate ground for such

small species and young molluscs. Nevertheless, mi-

crohabitats provide young individuals and small-sized

species with a twofold advantage: on the one hand,

they lessen the mortality risk, on the other hand, they

supply abundant food. In fact, C. pileare individu-

als even attach themselves to the algae by means of

the shell villi (Gosselin and Chia, 1995). It can be

stated that, throughout small spaces, the variety of

microhabitats is a factor contributing to the structural

complexity of the ecosystem as a whole.

Considering the feeding strategies, structurally di-

verse species with different specialization along thetrophic chain may live together within the same en-

vironment (Diaz, 1995). It is worth mentioning that

the Opistobranchia E. crispata is a specific feeder of

Siphonale algae. Also interesting are the cryptic mech-

anisms of epibenthic fauna to avoid predation (Ellison

and Farnsworth, 1990): the shells’ coloration of many

recorded organisms vary widely while others adopted

the color of the surrounding ground.

The three sites, under different degrees of anthro-

pogenic impacts, showed related values of species

richness, diversity and abundance, as well as densit-

ies of mollusc taxa in oceanic communities associated

with mangrove roots. Further research should be done

to find similar responses in accompanying significant

groups, such as Crustacea and Polychaeta.

Acknowledgements

This work was partially supported by COLCIENCIAS

Grant No. 428-97 for the project ‘Evaluacion de la

biodiversidad en las areas de manglar de San Andrés

y Providencia, Caribe colombiano’. The authors thank

A. Santos-Martinez for her comments and support, J.

Bonilla and C. Orozco for improving the English text

and the figures, respectively.

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