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Vol. 26, No 3, 4
Julio - Diciembre 2018
An International Refereed Scientic Journal
of the Facultad Experimental de Ciencias
at the Universidad del Zulia
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ISSN: 1315-2076
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
CIENCIA 26 (3,4), 63 - 73, 2018
Maracaibo, Venezuela
Does the marine macrobenthic community recover after an oil
spill? 10 years since the Nissos Amorgos disaster in Venezuelan Gulf,
Caribbean Sea
Héctor Severeyn
*1
, Yajaira García de Severeyn
2
, Mario Nava
1
, Félix Morales
3
.
Marynes Montiel M.
4
, Lisandro Morán.
1
Universidad del Zulia, Fac. Experimental de Ciencias, Departamento. de Biología
1
Lab. de Sistemática de Invertebrados Acuáticos,
2
Lab. de Cultivo de Invertebrados Acuáticos,
3
Lab. de Oceanografía,
4
Unidad de Microbiología Ambiental
Maracaibo, Zulia, Venezuela. *Email: hectorsevereyn@yahoo.com
Recibido: 04-07-2018 Aceptado: 28-07-2018
Abstract
In 1997, 25.000 barrels of petroleum were spilled along 40 Km of marine beaches in Venezuela Gulf, an area
where we carried out, two years before, benthonic macro invertebrates (BMI) inventories. In order to monitor
the ecosystem “recovery”, we repeated inventories ve (2003) and 10 years (2008) later. Before the spill (1996),
the BMI community was constituted by 75 species: 30 gastropod mollusks (GM), 28 bivalve mollusks (BM), 11
annelids (A) and 6 crustaceans (C). After ve years this community structure became 27 GM, 26 BM, 5 A and 3
C. Although biodiversity only decreased 16.7% (14 species), the composition changed: out of the 75 BMI before
the spill, only reappeared 31% (11 BM, 7 GM, 3 A and 2 C). After 10 years, the BMI biodiversity increased by a
factor of 1.5 (113 species) respect to 1996. Community structure changed to 48 BM, 36 GM, 14 C and 13 A, plus
2 new echinoderm species. Out of these 113 species only 38 were original species (OPS) before the oil spill (16
BM, 15 GM, 3 C and 2 A). Therefore, 51% of the OPS remained without returning. Our results contradict the
classic statement about marine ecosystem recovery aected by oil spills, i.e. to return to its “original condition”
are required 2-5 years. Indeed, this investigation indicates that recovery of Caño Sagua BMI community may
take, at least, one more decade. But, will the BMI return to their original condition? The probability is extremely
low. The most likely scenario will be, at a time dicult to estimate today, a new assemblage of BMI species in
equilibrium, with a mixture of OPS and new ones. These results means that, in terms of the original ecosystem
condition, the BMI community of Caño Sagua beach, never will recover since its trophic structure never will be
the same.
Keyword:
oil spill, macroinvertebrates, benthos, recovery, trophic structure, Venezuela Gulf, marine
ecosystem.
¿Se recupera la comunidad macrobentónica después de un derrame petrolero? A
10 añ
os del desastre del Nissos Amorgos en el Golfo de Venezuela, Mar Caribe
Resumen
En 1997, 25.000 barriles de petróleo fueron derramados a lo largo de 40 Km de playas marinas en el Golfo de
Venezuela, una zona donde dos años antes se habían realizado inventarios de macroinvertebrados bentónicos
(BMI). Con el objetivo de monitorear la recuperación del ecosistema se repitieron los mismos inventarios a los
cinco (2003) y 10 años (2008). Antes del derrame la comunidad de BMI estuvo constituida por 75 especies:
30 moluscos gasterópodos (GM), 28 moluscos bivalvos (BM), 11 anélidos (A) y 6 crustáceos (C). Después de
cinco años la estructura de la comunidad cambió a 27 GM, 26 BM, 5 A y 3 C. Aunque la biodiversidad solo se
redujo en 16.7% (14 especies), la composición cambió ya que de 75 BMI antes del derrame, solo reaparecieron
el 31% (11 BM, 7 GM, 3 C y 2 A). Después de 10 años, la biodiversidad de BMI aumentó en una proporción de 1.5
(113 especies). La estructura de la comunidad cambió a 48 BM, 36 GM, 14 C y 13 A, más 2 especies nuevas de
DOI: https://www.doi.org/10.5281/zenodo.5590842
64 Does the marine macrobenthic community recover after an oil spill?...
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
Introduction
Since the last three decades of the XX century,
mankind observed a huge amount of petroleum
spills in the world aquatic environments, product
of exploration, exploitation and international trade
exportation of this mineral at worldwide level (1).
Also, we witnessed the highest quantity of oil spilled
into oceans peaked between 1974 and 1979 when
there was an average of 78.8 spills/year (1). Despite
the exploitation and transport of petroleum has not
diminished, it has been observed a reduction of the
number of spills, due to the enforcement of new
restrictions and regulations. Thus, between 2010
and 2017 the yearly average of oil spill decreased to
6.8 spills/year, but huge oil spills still occur, such as
the Deepwater Horizon oil spill, which released 4.9
million barrels of oil covering more than 1700 Km
of shores (2). The presence of petroleum in nature
constitutes a threat for all organisms, and especially
for aquatic ones that live in those environments
where have been occurred most of the largest oil
spills in our whole history (3).
According to several authors (4-6) most marine
ecosystems exposed to huge quantities of raw
petroleum that have been studied, require between
2 and 5 years for their recovery. However, this
concept of “recovery” is based essentially on the re-
colonization of the aected areas, without previous
knowledge of which species were there present
and even less whether or not, the previous trophic
structure has changed. Even nowadays, there are
authors applying the same concept (7-9) without
considerations about the kind of habitat being
aected, the guilt structure and the persistence of
oil inside the substrate aected. Thus, conclusions
about the recovery time of an ecosystem aected
by oil spills are based on misguided premises and
supported, most the time, only on post impact
studies (10-13).
Venezuela, the thirst largest oil producer country
of the world until 2002, was the site for massive oil
spills and they are still occurring (14). In eect, a
25.000-barrel oil spill happened in Venezuela Gulf
in 1997. This spill covered 40 Km of marine coast,
killing every aquatic invertebrate between the low
and high tide lines (15). Because two years before
(1994-1996), we performed a two years biodiversity
inventory of benthonic macroinvertebrates (BMI)
along the same area, an invaluable opportunity rose
to measure the direct impact of this oil spill, starting
from ecological pristine conditions. Thus, we not only
made estimation of the number of species aected
and the quantify of the total mortality of these
organisms but also, and more important, we also
make projections, in real time, of how many years
this ecosystem could take to totally recover. This
opportunity was also important because Caño Sagua
beach is a tropical high energy sandy beach, one of
the few where an oil spill has happened and where
an exceptionally high diverse macroinvertebrate
benthonic fauna was known before it (15).
The macroinvertebrate fauna (organisms
retained by 500mm mesh sieve) of sandy beaches
is important because of their size and its ecological
role as relevant preys to higher trophic levels (16).
This macrofauna have some adaptations that remark
its trophic role: 1) planktonic larval development
able to be disperse; 2) one or more years of
generation times; 3) iteroparous reproduction and
continuous growth; 4) feeding on a broad range of
particles size; and 5) most of them motile (17). This
assemblage is normally formed by bivalve mollusks,
decapod crustaceans, polychaetes, amphipods,
and isopods, with low number of species, no
more than 20. However, in Caño Sagua beach the
macroinvertebrate fauna is four times that number
with an uncommonly high number of gastropods
mollusks.
In the present article we aim to answer the
following questions: How did the spill of petroleum
aect the biodiversity of BMI of the marine coast of
Caño Sagua beach, located at the southwestern of the
Venezuela Gulf? How many species disappeared?
How much time the BMI community will take to
equinodermos. De las 113 especies, solo 38 eran especies originales (OPS) desde antes del derrame de petróleo
(16 BM, 15 GM, 3 C y 2 A). Por lo tanto, 51% de las OPS se mantuvieron sin regresar. Los resultados obtenidos
contradicen la clásica armación acerca de la recuperación de ecosistemas marinos afectados por derrames de
petróleo, i.e. para regresar a la “condición original” son necesarios de 2 a 5 años. En efecto, esta investigación
indica que la recuperación de la comunidad de BMI de Caño Sagua se pudiera llevar, al menos, una década más.
Pero, ¿volverán los BMI a su condición original? La probabilidad es extremadamente baja. El escenario más
probable será, en una cantidad de tiempo difícil de precisar hoy, volver a una nueva estructura de BMI especies
en equilibrio, con una mezcla de OPS y otras nuevas. Estos resultados signican que, en relación a la condición
ecológica original, la comunidad de BMI de la playa de Caño Sagua no se recuperará debido a que su estructura
tróca nunca será la misma.
Palabras claves: Derrame de petróleo, macroinvertebrados, bentos, recuperación, estructura tróca, Golfo
de Venezuela, ecosistema marino.
65Severeyn et. al.,/ Ciencia Vol. 26, Número Especial (2018) 63-73
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
recover? It has been enough 10 years? In addition,
we explore the concept of “recovery” looking for the
best way to dene, to in ecological terms, what this
term really means.
Material and methods
The present study was carried out in the beach
Caño Sagua, located to 80 Km. of the city of
Maracaibo, in the Southwestern area of the Gulf
of Venezuela (Fig. 1). This coastline was the main
zone aected by the Nissos Amorgos Tanker oil
spill. This entire coastal zone, 40 Km of a tropical
high energy sandy beach, has a broad intertidal at
(100 m between high and low tide borders) which
uncovers twice every to 24 hours. The supra tidal
area plus the intertidal one, were covered by a thick
layer of petroleum which was estimated in 15.000
barrels (15). It was calculated that 9.000 barrels,
covered the bottom of the subtidal zone at least for a
year. After, there was neither other measurement of
this oil cover nor any monitoring of the evolution of
the disintegration of petroleum remains.
Before of the oil spill (1994-1995), six months
after the oil spill and them at 5 (2003) and 10
years (2007), we proceeded to carry on a yearlong
biodiversity inventory following the sampling
methodology with transect and quadrant, the same
that was used for the before spill inventory (15). This
consisted on tracing a perpendicular 100 m transect
to the beach beginning at the low tide line. Along the
transect, each 10 m, three samples were collected
(replicates) perpendicular to it, each separated
by two meters. Each sample was pull out with an
Ekman grab, collecting 0.01 m
2
(approximately 2
pounds of sand) and placed in plastic bags.
Figure 1. Geographic location of the Nissos Amorgos oil spill along the southwestern coast
of Venezuela Gulf. Arrows indicate the course of oil spread.
The collected sediment samples, were
transported by car to the laboratory where they were
sieved through a series of nets (180 microns up to 2
mm). The organisms retained by the dierent sieves
were sorted with forceps, separated by Fila and later
on identied to the lowest taxonomy category (39-
43). All organisms were xed in 10% formalin and
preserved 24 hours later in a 70% buered ethanol
solution.
The BMI data used and discussed in this paper
were collected, processed and analyzed by the
methodology above described during 1994-1995
(two year before the oil spill), 2002-2003 (ve years
after the oil spill) and 2007-2008 (10 years after
the oil spill). The discussion only will employ the
list of species (Biodiversity level 1) that were found
during a standardized year of intensive collection
that gather 360 individual samples, to support the
premise that “recovery” from an oil spill cannot
be state using increases of absolute abundances
and ecological diversity indexes. We intentionally
did this because it has been demonstrated that the
extreme variation of organisms abundance and
density in space and time, which appear to be real,
does not allow to separate background variation
66 Does the marine macrobenthic community recover after an oil spill?...
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
from impact changes (18-20). Thus, we just want to
proof that after ten year, the species arrangement of
the macroinvertebrate fauna has not showed up to
the original, pristine composition.
Results
Out of 75 BMI species quantied before the oil
spill, 58 were mollusks (30 gastropods, 28 bivalves),
11 annelids and six crustaceans (Fig. 2, Table 1). Six
months after the oil spill a brief sampling was done
but no living organisms were found. The process to
collect coastal oiled sediments, oil contaminated
debris and meteorized solid mass of petroleum took
almost a year (1998) but because 9000 oil barrels
sunk close to the coast, they generated a continuous
ow of oil fractions at least for one more year.
Beaches along the 40 Km aected were open to
tourist two year after (2000) but patches of sand-
oil were seeming until late 2001. By the time of the
rst formal biodiversity survey, ve year after the
oil spill, no meteorized solid masses were seen. At
this time, BMI community became structured by 61
species (27 gastropods, 26 bivalves, 5 annelids and
3 crustaceans) (Fig. 3, Table 2) (15). The fact that
after ve year the number of species of the BMI
community were still below the initial amount (75
vs 61) clearly indicated that the impact of the oil
spill has not nished yet. Notwithstanding, in term
of number of species, there was a reduction of 14
species (19%), the composition changed completely.
If we consider the species that were initially (Table
1), only 11 bivalves, 7 gastropods, 3 crustaceans
and 2 annelids came back in ve years (Table 2).
We can infer that the return to the original species
arrangement still remain at 31% (23 species out of
the original 75). In other words, 69% of the original
species have not came back.
Figure 2. Macrobenthic Invertebrate
fauna of Caño Sagua beach before the
Nissos Amorgos oil spill (1994-1995)
Figure 3. Macrobenthic Invertebrate
fauna of Caño Sagua beach, after ve (2003)
and 10 years (2008), of the Nissos Amorgos
oil spill
Table 1.- Species list of benthonic macroinvertebrates of Caño Sagua beach before the
Nissos Amorgos oil spill (1996).
Bivalves Gasteropods Crustacean Annelids
Anadara brasiliana Alaba incerta Emerita brasiliensis Hemipodus sp.
Anadara oridana Anachis sp. Excirollana braziliensis Leanira sp.
Brachidontes sp. Antigona sp. Lepidopa sp. Lumbrineris sp.
Chione cancellata Bittium sp. Liljeborgia sp. Malacocerus sp.
Codakia orbicularis Cerithiopsis latum Ogyrides alphaerostris Pilargidae sp. 1
Codakia orbiculata Cirsotrema dalli Penaeus sp Pisionidens sp.1
Codakia pectinella Cochliolepis parasitica Polychaet sp 1
Crasinella lunulata Cresseis acicula Polychaet sp sp 2
Crassostrea rhizophorae Diastoma varium Polychaet sp 3
Cyrtopleura costata Diodora sp. Polychaet sp 4
Diplodonta sp. Epitonium frielei Spio sp
Donax denticulatus E. novangliae
Donax striatus E. turritellarum
Ervilia concentrica Eulima bifasciata
67Severeyn et. al.,/ Ciencia Vol. 26, Número Especial (2018) 63-73
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
Gemma purpurea Fontigens turritella
Macoma breviformis Marginella sp.
Mulinia lateralis Melongena melongena
Mytilus sp. Microdochus oridanus
Petricola pholadiformis Mitrella nitens
Pholas campechiensis Natica canrena
Pitar dione Odostomia sp
Pteria sp. Olivella minuta
Rangia cuneata Petaloconchus erectus
Strigilla pisiformis Pseudomalaxis nobilis
Tellina exilis Serpulorbis sp.
Tellina radiata Solariella obscura
Tivela mactroides Teinostoma sp.
Transennella cubaniana Truncatella sp.
Turbonilla sp.
Vitrinella sp.
28 30 6 11
Table 2.- Species list of benthonic macroinvertebrates of Caño Sagua beach ve year after
the Nissos Amorgos oil spill (2002). In bold are the original species since 1996
Bivalvia Gasteropoda Crustacean Annelida
Anadara ovalis Alaba incerta Liljeborgia sp. Capitella capitata
Anadara sp. Alvania arpa Emerita brasiliensis Malacocerus sp
Chione cancellata Anachis obesa.
Excirollana
braziliensis
Pilargiidae
Chione granullata Antigona sp. Pisionidens sp 1
Circulus multistriatus Antipoda sp Serpulloides decussata
Crassostrea rhizophorae Bittium varium
Crassotrea virginica C. costata
Cyrtopleura costata Cerithiella whiteavessis
Donax denticulatus Cerithiopsis emersoni
Donax striatus Ciclostremiscus trilix
Heliacus bisulcatus Epitonium candeanum
Mitrella nitens E. foliacercostatum
Mulinia lateralis Heliacus sp
Mytilus sp. Hidrobia sp
Nuculana acuta Hyalina sp
Pitar dione Marginella sp.
Pteria sp. Natica canrena
Strigilla carnaria Natica menkeana
Strigilla pisiformis Odostomia laevigata
Tellina provina Olivella minuta
Tivela mactroides
Petaloconchus
irregularis
Crassinella martinicensis S. decussatta
Gouldia cerina Thais sp
Pecten sp Tricolia adamsi
Brachidontes modiolus Truncatella caribaensis.
Corbula sp. Turbonilla sp.
Zebina browniana
26 27 3 5
68 Does the marine macrobenthic community recover after an oil spill?...
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
The results 10 years after the oil spill shows
a more dramatic panorama in term of the BMI
community structure. First of all, there was a
huge increase of the number of species. The BMI
community reached almost twice of the number of
species before the oil spill (75 vs 113; Fig. 4, Table 3).
These 113 species were 48 gastropods, 36 bivalves,
14 crustaceans, 13 annelids and a new taxonomic
group, very uncommon in these high energy sandy
beaches, echinoderms, with two species.
Figure 4. Comparison of Macrobenthic Invertebrate fauna of Caño Sagua beach, before
(1996), after ve (2003) and 10 years (2008), of the Nissos Amorgos oil spill.
Table 3.- Species list of benthonic macroinvertebrates of Caño Sagua beach ten year after
the Nissos Amorgos oil spill (2007). In bold are the original species since 1996.
Bivalve Gasteropods Crustacean Annelida Echinoderms
Americardia guppyi Alaba incerta Amphipod sp 1 Aphroditidae sp 1 Sea urchin sp 1
Anadara notabilis
Anachis
mangelioides
Copepod
harpacticoide
Capitela capitata Ophiuroidea sp 1
Anadara ovalis Arene cruentata Brachyura crab sp 1 Gliceridae sp 1
Anadara transversa Assiminea succinea Caprellidae sp 1 Heteromastus sp
Arca imbrincata Caecum antillarum
Emerita
brasiliensis
Lumbrineris sp
Brachiodontes
exustus
Caecum imbrincatum
Excirolana
braziliensis
Onuphidae sp 1
Corbulla contracta Circulus multistriatus Haustoriidae sp 1 Orbiniidae sp 1
Crassinella
lunulata
Crepidula convexa Mithrax sp1 Polichaeta sp 1
Crassostrea
rizhophorae
Cyclostremicus
pentagonus
Ogyrides
alphaerostris
Polichaeta sp 2
Cyrtopleura
costata
Cyclostremicus sp 1
Parguristes
puncticeps
Polichaeta sp 3
Diplodonta no-
tata
Cyclostremicus sp 2
Processidae sp 1
(shrimp)
Sigalionidae sp 1
Donax denticu-
latus
Cyclostrema cance-
llatum
Tanaidacean sp 1 Spio sp 1
Donax striatus Cylichna auberi Tanaidacean sp 2 Sygambra sp 1
Ervilia
concentrica
Diastoma varium Tanaidacean sp 3
Gemma purpurea Diodora sp 1
69Severeyn et. al.,/ Ciencia Vol. 26, Número Especial (2018) 63-73
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
Lucina muricata Epitonium albidum
Macoma constricta
Epitonium
candeanum
Mactrellona alta
Epitonium
foliaceicostum
Martesia sp 1
Epitonium
novangliae
Mulinia lateralis
Epitonium
turritellulum
Musculus lateralis Eulima bifasciata
Mytella sp 1 Gastropod sp 1
Mytilopsis
dominguensis
Gastropod sp 2
Nuculana acuta Gastropod sp 3
Periploma sp 1 Haminoea succinea
Pholas
campechensis
Hidrobia sp 1
Pitar dione
Ithycithara
lanceolata
Pteria sp. 1 Litiopa melanostoma
Semele nuculoides Marissa cornuarietis
Sphenia antillensis Melanella sp 1
Strigilla
pisiformis
Melongena corona
Tellina sp.1
Microdochus
oridanus
Tivela
mactroides
Mitrela nitens
Trachycardium
muricatum
Natica carenna
Trachycardium sp1
Odostomia
laevigata
Transenella
cubaniana
Olivella dealbata
Olivella minuta
Olivella petiolita
Parviturboides
interruptus
Petaloconchus
erectus
Polinices sp 1
Pseudomalaxis
nobilis
Retusa candei
Serpulorbis
decussata
Tricolia adamsi
Turbonilla sp1
Turritella variegata
Vitrinella sp 1
36 48 14 13 2
70 Does the marine macrobenthic community recover after an oil spill?...
Scientic Journal from the Experimental Faculty of Sciences,
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This apparent “recovery”, as a function of number
of species, masks the true alteration of the original
condition of the aquatic ecosystem in Caño Sagua
beach. If it is compared the community of BMI
before the spill and 10 years later, in terms of the
species that originally were present, it is observed
that the community changed. After 10 years only
16 bivalves, 15 gastropods, three crustaceans and
two annelids of the original species, have returned.
These 38 species, representing a 51%, what indicates
is that in the last ve years (2003-2007) the original
BMI fauna of Caño Sagua recovered only 20% (51
less 31), a mean of 4% annually. Still, 49 % of the
species that used to live in Caño Sagua beach before
the spill of petroleum, remain missing.
In addition, as a consequence of the missing
species, an immense quantity of opportunists
species (66 species, Table 3) move into Caño Sagua
beach ecosystem to compete for a place (i.e. a niche).
These niches were left empty by the species that
disappeared.
Discussion
Coastal invertebrates’ studies on the eects of
oil spills, on dierent bottom-dwelling invertebrate
groups, have to a large extent been based on data
where there is not direct comparisons between pre-
spill and post-spill. In eect, there are many reports
that used toxicity tests laboratory experiments
to proof, whether or not, chemical derived from
petroleum (and their concentrations), may aect
(death) organism living within the areas covered by
the spills (21). Other studies used eld or laboratory
microcosms containing oiled sediments to verify
how the spill could aect the growth rate of larval
stages, juveniles and adults, and then extrapolate
the results comparing, less oiled, most oiled as well
as unexposed sediments/organisms, correlating
oil concentration and growth rates (22-23). Other
researchers, use comparisons of the fauna in
aected sediments by the spill versus sediments in
other zones no aected and, with the assumption,
that these last zones are “pre-spill ones” (24-
26). All above examples, of an incorrect way to
estimate oil spill impacts, what have created is an
unprecedented confusion and wrong expectations
when mankind has had to deal with the destruction
of our environment, in the present case, our oceans.
We want to believe that no matter what we do,
always nature will return to the former equilibrium,
which nature achieved in thousands or millions of
years, in a few of years. Due to this, not only we have
an incorrect estimation of how many years will be
necessary, but also that the arrangement, the trophic
structure and the ecological equilibrium, never
more will be the same. Examples of the above false
expectation abundance such as the recovery, in six
years, of Korean coasts after a 10.900 ton of crude
oil from the Hebei Spirit (27) (see 4-6 for similar or
lower times).
An additional mistake when analyzing oil spill
is to compare dierent habitats and dierent
organisms. There is no way to contrast oil spill
in salt marshes, wetlands, mangroves, estuaries,
marine coastal habitat and coral reef. Each of these
“environment” has dierent attributes, physico-
chemical features, and biota. An example of a
huge oil spill that aected all those habitats is the
Deepwater Horizon mega oil spill (28) and where
there are, separate formally, oil impact studies in
each of these environment/habitats (29-33).
In relation with the present article, it is
important to point out that the Nissos Amorgos oil
spill occurred in a high energy sandy marine beach,
under tropical conditions, which is very unusual.
Most oil spill that has taken place in sandy beaches,
were in subtropical or temperate zones. Eectively,
in a recent revision (34, see Table 1) is remarked
that only 17 oil spills, that were documented,
occurred in coastal sandy shores between 1973 and
2016. Although our literature review found some
more articles, it is important to note that any of
them coincide with our study. In fact, seven studies
were done only with meiofauna (invertebrates size
between 45 microns and 1 mm), two with both
meiofauna and macroinvertebrate fauna, but in
temperate zones (Spain and United Kingdom). From
the resting six studies, three documented the oil
spill impact only over the macrofaunal amphipods
community; one in subtropical (Sidney, Australia),
the second one in temperate latitudes (Paranagua
Bay, Brazil), and the third in tropical conditions
(Puerto Rico) but it did not include other important
macrofaunal organisms and it was concentrated on
sandy sediments within mangroves. Thus, the last
three studies, notwithstanding reported the oil spill
impact over important macrofaunal components
(crustacean, annelids and mollusks), two of them
occurred in temperate conditions (Alaska, US and
Campeche, Mexico). So, from the 17 oil impact
studies mentioned, only one (35) came about in
very similar condition as our in Caño Sagua beach,
but only included amphipods and crabs because no
other organisms were found.
The above discussion about oil spill impact
studies developed in sandy beaches had the only
objective to re-emphasize the relevance of the
present paper for the Caribbean region and tropical
ecosystems in general. Recent articles (36-37) have
emphasized the potentially dangerous situation of
the whole Caribbean region where more than 30
oil spills occurred during the 70s, plus “countless
mundane releases of petroleum from ships and
shoreline facilities” (36). This enclosed sea is ranked
71Severeyn et. al.,/ Ciencia Vol. 26, Número Especial (2018) 63-73
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
as having one of the most intense maritime trac
in the world (37) and, at the same time, it is the
supports of many critical habitats functioning as a
large marine ecosystem (38). In most cases, all these
accidents aected coral reef, mangroves and their
ora and fauna. But it is clear that high energy sandy
beaches are potential targets in future decades.
Now, are our results unexpected? No really.
Several studies have shown that, after an oil spill
impacts, the fauna that reappear follows a two steps
pattern (34). First, it is the disaster phase where
everything alive is destroy. When “recovery” begins,
a second phase take place where species which were
present before the spill, start to appear. Then comes
a phase that is characteristically evidenced by the
arrival of new species that do not existed before
the oil spill. These new species are considered as
“opportunistic” (34-36). The reason of their generic
names is obvious, as they get the chance to occupy
niches that were left empty by the species killed by
the oil spill. We saw clearly these three phases as
a sequence in our 12 years study, presented in the
above lines.
As we stated at the beginning of this article, the
results obtained contradict the classic statements
about the ecosystem recovery time after an oil spill:
to return to its original condition as function of
diversity and abundance of the present species,
between two and ve years are necessary (4-6).
On the contrary, the present data indicates that the
ecosystem of Caño Sagua beach, studied through
the changes in the community of BMI, would take
more than two decades in returning to the original
species composition. This time, is at least between
6 and 15 times longer than those mentioned in the
scientic literature reviewed in the present article.
Indeed, this study demonstrates that 10 years after
the impact of the oil spill, only have returned 38
species, 15 of them in the last 5 years (2003-2007).
If we project these numbers (a gross rate of 10
species every 5 years) the BMI community of Caño
Sagua should return to its original condition in 20
more years. These years, added to the 10 already
lapsed, tell us about of a total time of 30 year for the
recovery.
Now, to nish this discussion let us take
another side of the “recovery concept”. Taking into
account what we have seen, can we arm that the
BMI community of Caño Sagua can return to its
original structure? We must begin, conceiving that
this recovery only could happen in a hypothetical
situation where the niches left vacant, can be re-
colonized by the same species that existed before
the oil spill. Indeed, the results indicate that after
10 years there are 76 new species competing for
approximately 35 niches (75 in 1996 less 35 in
2003). In other words, approximately two new
species, are already competing versus an old one
that has not returned yet in 10 years. Is it likely that
this event may happen? Denitely the answer is no.
Everything indicates that, in terms of the original
condition of the ecosystem, Caño Sagua beach will
never recover. This is the paradox and the take-
home message that this investigation contributes.
Many studies that have investigated the eect of
oil spill, at some point, have used the phrase “the
ecosystem is showing sign of recovery” or other
similar (5-8). However, we can state that the
impacts taken place against the nature by mankind
are likely irreversible. The thousands or millions
of years that nature has taken in developing stable
ecosystems and their trophic nets cannot recover in
just some decades after the imbalance introduced by
man. As an alternative, nature will look for to reach
a new balanced, in equilibrium stage, with a similar
number of species to the original ones, but with a
mixture of old and new species. This means that the
trophic net never will be the same.
Although the knowledge about the eects of
major oil spills on marine and coastal ecosystems
has improved considerably in last decades, there
are still critical research needed for questions
that remain unresolved or are poorly understood.
One key point at this respect is that we need to
leave the approach of using non-impacted areas
biodiversity, abundances and ecological indexes,
to obtain likely numbers for oil impact of unknown
results. Bases lines studies and regular inventories
in areas, zones or habitat that are potential target for
oil spill must be the strategy in order to be prepared
for the future (34).
Bibliographic references
1.ITOPF. Global Tanker Spill Trend. 2018.
2. SIVANESAN S. Disaster Advances. 6: 1-3, 2013.
3. BEYER H., TRANNUM C., BAKKE T., HODSON P,
COLLIER T. Mar. Poll. Bull. 110 (1): 28-51,
2016.
4. YAMAMOTO T., NAKAOKA M., KOMATSU T.,
KAWAI H M., OHWADA K. Mar. Poll. Bull.
47:1-6, 2003.
5. NIKITIK C., ROBINSON A. Mar. Poll. Bull.
46:1125-1141, 2003.
6. SKALSKI J., COATS D., FUKUYAMA A. Environ.
Manag. 28:9-18, 2001.
7. HOUGHTON J., FUKUYAMA A., LEES D.,
HAGUE P., CUMBERLAND H. Evaluation
of the condition of Prince William
sound shoreline following the Exxon
72 Does the marine macrobenthic community recover after an oil spill?...
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
Valdez oil spill and subsequent shoreline
treatment. Technical reports NOAA PB-96-
113287 (Vol. 1) and NOAA PB-96-113303 (vol.
2), National Ocean Service, Seatle, Washington.
1993.
8. MATISHOV G., INZHEBELKIN Y., SAVITSKII R.
Water Res. 40: 259-273, 2013.
9. MACCALL B., PENNINGS S. PLoS ONE. 7:3273,
2012.
10. KOYAMA J., UNO S., KOHN O. Mar. Poll. 49:
1054-1061, 2004
11. PETERSON C., ESTES J. (2001) Conservation
and management of Marine Commu-
nities. Pp. 469-507, in Bertne M., Gaines
S., Hay M. (eds.) Marine Community
Ecology. Sinauers Associates Inc, Sunderland,
Massachusetts, USA, 2001.
12. DAY R., MURPHY N., SMITH G., WIENS D.,
HAYWARD D., HARPER J. Ecol. Applic.
7:593-613, 1997.
13. PAINE R., RUESINK E., SUN E., SOULANILLE
M., WONHAN C., HARKEY C., BRUMBAUGH
D., SECORD D. Ann. Rev. Ecol. Syst. 27:197-
235, 1996.
14. WIKIPEDIA. History of the Venezuelan oil
industry, Wikimedia Foundation, Inc., 2016.
15. SEVEREYN H., DELGADO J., GODOY A., GARCÍA
DE SEVEREYN Y. Ecotrópicos 16: 12-19,
2003.
16. SCHLACHER T., SCHOEMAN D., DUGAN
J., LASTRA M., JONES A., SCAPINI F.,
MCLACHLAN A. Mar. Ecol. 29: 70-90, 2008.
17. WARWICK R., CLARKE K. Oecologia 61: 32-41,
1984.
18. DIANA S., SOTO L., ESTRADAS A., BOTELLO A.
Mar. Poll. Bull.114: 987-994, 2017.
19. BAE H., LEE J., SONG S., RYU J. Environ. Poll.
241: 596-606, 2018.
20. NAVA M., SEVEREYN H. 2010. Ciencia 18
(4):235-246, 2010.
21. KRASNEC M., MORRIS J., LAY C. An evaluation
of the toxicity of deep sea sediment
collected after the Deepwater Horizon
oil spill on the amphipod Leptocheirus
plumulosus. Tech. Working Group Report.
Boulder, CO, USA, 2015.
22. ROZAS L., MINELLO T., MILES M. Estuar.
Coast. 1:1-12. 2014.
23. GREY E., CHIASSON S., WILLIAMS H., TROEGER
V., TAYLOR C. Plos One 10:19, 2015.
24. WASHBURN T., RHODES A., MONTAGNA P.
2016. Ecol. Indicat. 71: 587-597, 20.16
25. FANGYUAN Q., NUNNALLY C., LEMANSKI
J., WADE T., RAINER M., ROWET A. Deep
Sea Res. DOI: ttp://dx.doi.org/10.1016/j.
dsr2.2015.04.020, 2015.
26. FOSTER J., WICKSTEN M., DAVENPORT C.,
SOLIMAN R., WANG Y. Mar. Ecol. Prog.
Ser. 399: 1-14, 2010.
27. YUN-HWAN J., HENUG-SIK P., KON-TAK Y.,
HYUNG-JUNE K., WON-JOON K. Ocean
Sci. J. 52: 103-112, 2017.
28. MICHEL J., OWENS E., ZENGEL S., GRAHAM
M., NIXON Z., ALLARD T., HOLTON W.,
REIMER D., LAMARCHE A., WHITE M., CARL
N., CHILDS G. MAUSETH G., CHALLENGER
E., TAYLOR M. PLoS ONE 8(6): 65087, 2013.
29. DELAUNE R., WRIGHT A. Soil Sci. Soc. Am. J.
75: 1602-1612, 2011.
30. SANTOS H., CARMO F., PAES J., ROSADO A.,
PEIXOTO R. Water Air Soil Poll. 216: 329-
350, 2011.
31. MENDELSSOHN I., ANDERSEN G., BALTZ D.,
CAFFEY R, CARMAN K., FLEEGER J., JOYE
S., LIN QX., MALTBY E., OVERTON E., ROZAS
L. Bioscience 62: 562-574, 2012.
32. MCGENITY T. 2014. Curr. Opin. Biotech. 27:
46-54, 2014.
33. SNYDER R., VESTAL A., WELCH C., BARNES
G., PELOT R., EDERINGTON-HAGY M.,
HILEMAN F. Mar. Poll. Bull. 83: 87-91, 2014.
34. BEJARANO A, MICHEL J. Environm. Poll.
218:709-722, 2016.
35. CHAN E. 1976. Oil Pollution and Tropical
Littoral Communities: Biological Eects
of the 1975 Florida Keys Oil Spill. University
of Miami, Rosenstiel School of Marine and
Atmospheric Science, pp. 539-542, 1976.
36. BOND D. Comp. Stud. Soc. Hist. 59(3):600–
628, 2017.
37. SINGH A., ASMATH H., LEUNG C., DARSAN J.
Mar. Poll. Bull. 93 (2015) 217–227, 2015.
73Severeyn et. al.,/ Ciencia Vol. 26, Número Especial (2018) 63-73
Scientic Journal from the Experimental Faculty of Sciences,
at the Universidad del Zulia Volume 26 Especial N° 3, 4, Julio - Diciembre 2018
38. SHERMAN, K. Environ. Dev. 11: 43–66., 2014.
39. ABBOTT R. T. American Seashells. Second
Edition. Van Nostrand Reinhold Co., New York,
USA.663 p., 1974.
40. DÍAZ J. & M. PUYANA (1994). Moluscos del
Caribe Colombiano. Colciencias y Fundación
Natura. Bogotá, Colombia. 284 p., 1994.
41. RODRIGUEZ G. Crustáceos Decápodos
de Venezuela. Instituto Venezolano de
Investigaciones Cientícas. Caracas, pp 494,
1980
42. KENSLEY B. SCHOTTE M.Guide to marine
isopods crustaceans of the Caribbean.
Smithsonian institution press. Washington and
London. 308 p., 1989.
43. FALCHAUD K. The polichaete worms
denitions and keys to the order, families
and genera. Science series No 28. Natural
History Museum of Los Angeles County.
Sciences series. United States of America, pp
188, 1997.
44.- SEVEREYN H., NAVA M., GARCIA DE
SEVEREYN Y. Fish. Ocean. OAJ 3(5): 8 pp.
DOI: 10.19080/OFOAJ.2017.03.555625. 2017.
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