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 Estuarine, Coastal and Shelf Science 138 (2014) 101e106

Contents lists available at ScienceDirect

Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier.com/locate/ecss

Alien reef-building polychaete drives long-term changes in

invertebrate biomass and diversity in a small, urban estuary
K.A. McQuaid a, *, C.L. Griffiths a, b
a
Department of Biological Sciences, University of Cape Town, Rondebosch 7700, South Africa
b
Centre for Invasion Biology, University of Cape Town, Rondebosch 7700, South Africa

a r t i c l e i n f o a b s t r a c t

Article history: Two of the greatest threats to native biodiversity are the construction of artificial structures in natural
Received 11 July 2013 environments and the introduction of invasive species. As the development and urbanisation of estuaries
Accepted 24 December 2013 continues at an increasing rate worldwide, these environments are being simultaneously affected by
Available online 7 January 2014
these threats. This study quantifies the spread of an invasive reef-building polychaete, Ficopomatus
enigmaticus, in a small, highly manipulated urban estuary in South Africa and investigates its role as an
Keywords:
ecosystem engineer. Anthropogenic changes to the Zandvlei Estuary, including construction of a rubble
introduced species
weir and canalisation near the estuary mouth, construction of an extensive marina development and
ecosystem engineer
benthic fauna
hardening of the banks with concrete, have facilitated the expansion of F. enigmaticus. The standing stock
estuaries of F. enigmaticus increased from 13.69 t, as measured in 1986, to 50.03 t in 2012, due both to increase in
long-term changes the total area colonised and standing stock per m2. Since F. enigmaticus reefs support a greater biomass of
South Africa infauna than adjacent sandy areas, total invertebrate biomass in the estuary is estimated to have
increased from less than 0.30 t in 1942, to over 56.80 t in 2012, due mainly to hardening of banks in parts
of the main estuary with concrete and construction of a marina system. A positive correlation between
reef mass and infaunal biomass, density and diversity was also found.
Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction The reef-building polychaete Ficopomatus enigmaticus

Estuaries have become increasingly developed and urbanised
worldwide, as the human population continues to grow and the
popularity of coastal areas increases (Chapman, 2006; Blockley,
2007). Natural estuarine habitats are being replaced by man-
made ones, often leading to the formation of hard surfaces in
areas which were previously soft sand or sediment (Bulleri and
Airoldi, 2005; Chapman, 2006; Blockley, 2007; Glasby et al.,
2007; Dafforn et al., 2009). These artificial structures are then
colonised by a different fauna, often one dominated by non-
indigenous species (Bulleri and Airoldi, 2005; Glasby et al., 2007).
This can, in turn, further alter the habitat by creating new surfaces
and increasing habitat complexity, which will then influence the
abundance, diversity and distribution of associated organisms
(Coull and Wells, 1983). This world-wide phenomenon represents
the convergence of two of the greatest threats to native biodiver-
sity: habitat destruction and the introduction of non-indigenous
species (Glasby et al., 2007).
* Corresponding author.
E-mail address: kirstymcquaid@gmail.com (K.A. McQuaid).
(¼Mercierella enigmatica), belonging to the family Serpulidae, is an
excellent example of a highly invasive, habitat-modifying species.
F. enigmaticus is originally from Australia and has now been spread
around the world to colonise brackish waters in many tropical and
subtropical areas (Ten Hove and Weerdenberg, 1978; Day, 1981;
Fornós et al., 1997; Bianchi and Morri, 2001; Mead et al., 2011).
F. enigmaticus makes large reefs attached to hard substrata and
consisting of a dense network of calcareous tubes (Mead et al.,
2011). Neighbouring clumps of similar size may eventually join
together to form larger platforms several metres in diameter
(Obenat and Pezzani, 1994; Bianchi and Morri, 2001; Schwindt
et al., 2004a). Larval recruitment and growth rates are high and
individual worms may live up to several years (Bianchi and Morri,
2001).
Ficopomatus enigmaticus has been shown to have major impacts
on the systems it invades and is therefore considered an ecosystem
engineer (Schwindt et al., 2001, 2004b). In the Mar Chiquita coastal
lagoon in Argentina it has one of the strongest ecological effects of
all species introduced to the area (Schwindt et al., 2004a), changing
the physical environment by creating a complex network of tubes,
which create habitat for associated organisms and alter the physical
characteristics of the system (Coull and Wells, 1983; Schwindt et al.,

0272-7714/$ e see front matter Ó 2014 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecss.2013.12.016
102 K.A. McQuaid, C.L. Griffiths / Estuarine, Coastal and Shelf Science 138 (2014) 101e106
2001). The reefs are extremely important providers of shelter, food
and substratum for many different infaunal species and may also
affect interactions between native species, such as competition,
predation and parasitism (Obenat and Pezzani, 1994; Schwindt
et al., 2001, 2004b). Affected organisms include polychaetes, am-
phipods, juvenile crabs and gastropods (Schwindt and Iribarne,
2000; Schwindt et al., 2004b).
Over the past few decades there has appeared to have been a
great increase in Ficopomatus enigmaticus abundance in the
Zandvlei Estuary, Cape Town, South Africa. The Zandvlei is a
temporarily open/closed system which has been highly modified
and manipulated. Its catchment area on the southern slopes of
Table Mountain covers approximately 8500 ha and has been highly
developed and modified through human activities, including light
industry, housing, agriculture, forestry, conservation and com-
merce (Morant and Grindley, 1982; Davies et al., 1989; Brown and
Magoba, 2009; C.A.P.E., 2010b). As a result, Zandvlei now receives
low quality, high nutrient inflowing water (Morant and Grindley,
1982). Other major human-induced physical changes to Zandvlei
itself have included dredging of the estuary and reclamation of
surrounding fields, with subsequent stabilisation of parts of the
shore into steep concrete banks; canalisation near the estuary
mouth and associated installation of a rubble weir to stabilise water
levels; development of a complex, canalised marina system e the
‘Marina da Gama’ e and construction of a railway embankment that
cuts the headwater wetlands off from the rest of the estuary (Davies
et al., 1989; C.A.P.E., 2010a).
With the development of concrete walls along the banks of
Zandvlei in the early 1960s and excavation of the concrete-walled
canals of the Marina da Gama development in the 1970s, large
areas of hard substratum were created within a system which
previously comprised only soft sand and sediments. This facilitated
the invasion and expansion of Ficopomatus enigmaticus, which was
previously absent, or at least undetected, in the system, as there
had been little to no hard substratum available there for attach-
ment. The concrete walls, boats and jetties in the Zandvlei have
subsequently become increasingly covered in F. enigmaticus reefs,
leading to complaints from local canoeists and recreational users of
the estuary that the number and size of reefs have reached a point
where boat movement within some of the canals is now restricted
(C.A.P.E., 2010a). Despite these complaints, little work has been
done on F. enigmaticus within the Zandvlei Estuary, other than a
survey of its biomass within the Marina da Gama development by
Davies et al. (1989).
The primary aim of this study is to quantify the spread and
densification of the invasive polychaete, Ficopomatus enigmaticus,
by comparing its current distribution and abundance in Zandvlei to
those determined by Davies et al. (1989). The secondary aim is to
investigate its role as an ecosystem engineer, by surveying the
invertebrate communities associated with areas of reef and
comparing this to the fauna of uncolonised areas. No other organ-
ism within Zandvlei is found playing a comparable role as an
ecosystem engineers and its role in the estuary is thus unique.
2. Materials and methods
Sampling was carried out in the Zandvlei Estuary, 20 km south
of Cape Town, South Africa. The sampling methods followed, but
were modified slightly from, those carried out by Davies et al.
(1989). The perimeter of the estuary was divided into 200 m sec-
tions, including the Marina da Gama canals and all of the islands. In
sections where the banks were formed of concrete walls, one
random sample of Ficopomatus enigmaticus reef, approximately
0.0044 m2, was collected per section. Where the banks were of
untransformed sand, one sediment sample of the same size was
taken per section. This resulted in a total of 65 reef samples and 9
sediment samples. Samples were collected using a metal corer that
was pushed into the reef or sediment and pulled out to extract a
core sample. For each 200 m section an estimate of the percentage
cover (m2) of the wall by F. enigmaticus reef was made by eye and
the vertical height of the reef was recorded using a metre ruler.
Samples were taken back to the laboratory, where they were frozen
in water until processing.
After being defrosted, each reef sample was broken into smaller
pieces to release the infauna trapped between the polychaete
tubes. The infauna were then counted and identified under a dis-
secting microscope. This process was repeated with the nine
sediment samples. Between five and 100 individuals of each
infaunal species (depending on size) were oven-dried for 24 h at
70  C in order to obtain average individual mass per species and the
mean biomass of invertebrates per m2 of reef and sand was then
calculated as mean mass  density. The total infaunal biomass in
the Zandvlei was estimated by summing the biomass of infauna in
reef and that in soft sediment. For the reef samples, the mean
biomass of infauna per m2 of reef was multiplied by the number of
metres of concrete wall in that 200 m section and the mean depth
of the reef. For the sediment samples, the mean biomass of infauna
per m2 of sand was multiplied by section length (200 m) and then
by the mean length (m) of sand bank measured from the shore to a
depth of 0.6 m. This was done to account for the great decrease in
surface area available for infauna associated with transformation of
parts of the shore from a gentle, sloping, sandy bank into landfill,
edged by an almost vertical wall at a mean depth of 0.6 m.
The wet weight of Ficopomatus enigmaticus reef in each sample
was obtained using a top-loading balance and converted to dry
mass using a conversion ratio determined by oven-drying five
samples for 24 h at 70  C and calculating the mean ratio of wet
weight to dry weight. The biomass of F. enigmaticus in each 200 m
section was calculated by multiplying the mass in the core sample
up to 1 m2 and then multiplying this by the reef area in that section.
Finally, mass in each section was summed to obtain estimates of
total standing stock within the Marina da Gama development, and
then the estuary, as a whole. The mean total standing stock of
F. enigmaticus in the Marina da Gama can be compared with the
mean obtained for the same area by Davies et al. (1989). The sites
sampled in the Marina da Gama did not correspond exactly to those
sampled by Davis et al. (1989) because we chose to sample sys-
tematically once in every 200 m section, while Davis et al. (1989),
for unknown reasons, had several sites that were extremely close
together (Fig. 1). While F. enigmaticus does occasionally also attach
in low density to the submerged aquatic plant Potamogeton pecti-
natus and to hard objects on the bottom of the estuary, such as
rocks, logs, bottles and cans, these contributions to the total
biomass were considered negligible in relation to the large area of
reef on the concrete walls and were not incorporated in our esti-
mates of overall biomass.
The Davies et al. (1989) methods also differed in their calcula-
tions of total standing stock in the marina. When estimating the
surface area of the canal walls covered by Ficopomatus enigmaticus,
they simply used a mean depth of 2 m, based on the Morant and
Grindley (1982) description of the depth of the canals, and they
did not measure actual heights of the canal walls or reef. Pre-
liminary observations carried out in 2012 revealed a maximum reef
height of only 1.1 m, and hence the Davies et al. (1989) estimate of
surface area was therefore greatly over-estimated. This was
adjusted using the actual mean vertical reef height calculated in
this study, allowing for direct comparison between the two studies.
A further difference in the methods of these studies was that Davies
et al. (1989) used mean dry mass of reef per m2 to determine total
standing stock. In our study the biomass of each sample was used
 K.A. McQuaid, C.L. Griffiths / Estuarine, Coastal and Shelf Science 138 (2014) 101e106
Fig. 1. Zandvlei Estuary showing Marina da Gama canal system (extending from eastern bank) and sampling sites from (a) Davies et al. (1989) and (b) this study (2012). Maps
adapted from Davies and Stewart (1984).
along with its corresponding vertical reef height and percentage
cover to obtain separate totals for each 200 m section, which were
then summed.
Using the estimates of invertebrate biomass obtained in this
study, invertebrate biomass in the Zandvlei was back-calculated for
1942, prior to any major manipulation of the banks and for 1986,
when Davies et al. (1989) collected their samples. Historical maps
from the National Geospatial Information were used to estimate the
perimeter of the Zandvlei in 1942, before the dredging, stabilisation
of banks with concrete and development of the Marina da Gama
took place. At this time there were therefore no concrete walls and
the system consisted only of soft sediment. While there may have
been some changes to the fauna of these untransformed habitats
over time we consider it highly unlikely these would have been of a
magnitude that would be comparable to that caused by hardening
of the banks and the associated Ficopomatus enigmaticus invasion.
Invertebrate biomass in 1942 was thus calculated assuming that the
biomass per m2 and slope of the banks to a depth of 0.6 m in 1942
were the same as average values measured for those areas of the
estuary that remained untransformed in 2012. To estimate overall
biomass in 1986 we adjusted the Davies et al. (1989) measurements
for the Marina da Gama section, as explained above, and extrapo-
lated these figures to include concrete walls in the main section of
the estuary, assuming biomass per m2 of reef and percentage cover
at that time were the same as those reported in the marina area. To
this we added the biomass of untransformed sections of bank as
measured in 2012 (there having been no construction of additional
concrete bank over this period).
3. Results
The dry mass of reef was found to represent 46.15% (2.70, S.D.)
of total wet weight. Table 1 shows the mean, minimum, maximum
103
and total dry mass of Ficopomatus enigmaticus recorded in the main
estuary and Marina da Gama in 2012. The mean dry mass of
F. enigmaticus in the main estuary body was 6.66 kg m2  5.67 SD,
with a minimum of 0.05 kg m2 and a maximum of 17.66 kg m2. In
the Marina da Gama, these values were slightly higher, with a mean
dry mass of 8.05 kg m2  6.55 SD, a minimum of 0.25 kg m2 and a
maximum of 24.79 kg m2. The total area colonised by
F. enigmaticus in the main estuary was 843.4 m2, compared to
6138 m2 in the marina. The complex canal system of the marina
thus has a much larger surface area of concrete wall available for
colonisation than the main estuary, where much of the bank still
remains unhardened. Indeed, percentage cover of F. enigmaticus
reef on the banks of the marina was 98%, compared to only 30% of
the total bank in the main estuary. The total dry mass of
F. enigmaticus estimated in the main estuary was thus only 6.58 t,
compared to 50.03 t in the marina section, giving a total of 56.61 t
for the Zandvlei system as a whole.
The mean biomass of infauna per m2 of Ficopomatus enigmaticus
reef was 229.1 g m2  262.53 SD. Pearson productemoment
correlations showed significant correlations between reef mass and
infaunal biomass, infaunal density and number of infaunal species
Table 1
Mean, minimum, maximum and total dry mass of Ficopomatus enigmaticus in the
main Estuary and Marina da Gama in 2012, along with the number of square metres
colonised.
Main estuary body Marina da Gama
Mean dry mass  SD (kg m2) 6.66  5.67 8.05  6.55
Min dry mass (kg m2) 0.05 0.25
Max dry mass (kg m2) 17.66 24.79
No. m2 of F. enigmaticus 843.4 6138
Total dry mass (t) 6.58 50.03
104 K.A. McQuaid, C.L. Griffiths / Estuarine, Coastal and Shelf Science 138 (2014) 101e106

(p < 0.05). There was a significant trend of increasing infaunal invertebrate fauna over the past few decades. When Davies et al.
biomass (r ¼ 0.51) and density (r ¼ 0.43) with increasing reef mass carried out their study in 1986 the hardened banks of the marina
and a weaker, but still significant, positive correlation between had been present for approximately ten years. During that time the
number of infaunal species and reef mass (r ¼ 0.28). In the soft population of F. enigmaticus established within the Zandvlei, but
sand, the mean infaunal biomass was only 2.0 g m2  1.77 SD. A now, over 25 years later, the population has nearly quadrupled,
Wilcoxon Paired Sample Test showed a statistically strongly sig- indicating that the 1986 population was far from reaching the
nificant difference in the biomass of infauna associated with carrying capacity of the system. The great increase in F. enigmaticus
F. enigmaticus reef and sand (Z ¼ 3.41, p ¼ 0.0006). In addition, the is the result of both an increase in the mass of F. enigmaticus per unit
infaunal community associated with F. enigmaticus consisted of 16 area, and an increase in the total area covered by reef. In 1986 the
species, while only 10 infaunal species were found in the sand. mean dry mass of F. enigmaticus was 2.70 kg m2  2.1 SD, only a
Those absent from the sand, but present in the reef, included the third of the mean dry mass recorded in 2012, which was
estuarine snail, Tomichia ventricosa, two bryozoan species, 8.05 kg m2  6.55 SD. The total area colonised by F. enigmaticus
comprising one invasive and another unidentified species, and the had also greatly increased, from 5080 m2 in 1986 to 6138 m2 in
crown crab Hymenosoma orbiculare. Table 2 shows which species 2012. Davies et al. (1989) estimated a mean percentage cover of
were present in the reef and sand, as well as their relative bio- 73%  28 SD of the walls by F. enigmaticus, compared to 98% in this
masses. In all cases, except the Ceratonereis species, the biomass study. The total standing stock in the Marina da Gama in 1986, re-
was higher, often greatly so, in the reef than in the sand. calculated using the adjusted wall area, was thus 13.69 t, compared
Fig. 2 shows the Zandvlei at various stages of physical manip- to 50.03 t in 2012. Unfortunately, limitations in the historical data
ulation, indicating which parts of the estuary are sand and which set do not allow for statistical analyses of these results.
have been hardened. In 1942 there were no concrete walls and the While these increases seem substantial, in an international
total perimeter of the estuary was 7000 m, all comprised of soft context the invasion in the Zandvlei is far from reaching the high
mud or sand. The average width of the bank from the water edge to cover and production rates experienced elsewhere. In the Orbetello
a depth of 0.6 m, measured in 2012, was 21.1 m  13.36 SD. Total Lagoon, Italy, Ficopomatus enigmaticus is found over 2 km2 (Bianchi
biomass of infauna in the system in 1942 was therefore estimated and Morri, 2001), while in the Mar Chiquita coastal lagoon,
as 7000 m  21.1 m  2.0 g m2, which gave 0.30 t. By 1986 and Argentina, the reef covers up to 39.68 km2, representing 86.3% of
2012 the total perimeter of the Zandvlei had been expanded to the lagoon (Schwindt et al., 2001). These areas of reef are far more
approximately 17 000 m, having been greatly increased by the substantial than the 6138 m2 recorded in the Zandvlei. In the Mar
complex canal system associated with the Marina da Gama devel- Chiquita reef mass is centred on shells, which act as nuclei for
opment. In 1986 approximately 8468 m of bank was covered by growth on the floor of the estuary, rather than on banks or walls of
Ficopomatus enigmaticus, with 5354 m remaining as sand, and the the lagoon. While the population in this lagoon continues to grow,
total invertebrate biomass was estimated to have risen more than the rate of spread has decreased as less space and substratum is
40 fold to 14.33 t, including F. enigmaticus. Finally, in 2012, 11 846 m available (Schwindt et al., 2001). In Zandvlei F. enigmaticus reef
of wall was covered by F. enigmaticus reef with 5354 m remaining as grew at a rate of approximately 0.2 kg m2 y1, assuming constant
sand and total invertebrate biomass is estimated to have risen again growth rate, compared to an annual production of
by almost another four fold, to 56.80 t (Table 3). 21.269 kg m2 y1 in a coastal lagoon in Menorca, Spain (Fornós
et al., 1997). This raises questions as to whether F. enigmaticus has
4. Discussion reached carrying capacity in the Zandvlei Estuary, or whether the
population will still continue to expand.
Our results clearly show that manipulation and hardening of This study does, however, provide an excellent example of how
banks allowed the invasive reef-building polychaete Ficopomatus artificial structures can facilitate the introduction and proliferation
enigmaticus to proliferate in the Zandvlei and that this has resulted of non-indigenous species in estuarine environments. Although
in very large changes in both the biomass and composition of the Ficopomatus enigmaticus is widespread along the south and east
coasts of South Africa, there are few estuaries with suitable sub-
stratum to support its growth. Milnerton Lagoon is the only other
Table 2 estuary in the Western Cape where F. enigmaticus is abundant and
Mean biomass of species associated with F. enigmaticus reef and soft sand
here it is found in large clumps around a concrete bridge (pers.
(mean  SE).
obs.). F. enigmaticus has also recently established in the Berg River
Species Taxonomic group Biomass in Biomass in sand estuary, some 100 km further up the west coast of South Africa,
reef (g m2) (g m2)
following the construction of another marina in that system. Es-
Afrochiltonia capensis Order: Amphipoda 3.14  0.46 0.04  0.02 tuaries are particularly vulnerable to invasions by alien species as
Melita zeylanica Order: Amphipoda 33.18  8.55 0.48  0.32
they are not only being increasingly manipulated through the
Coropeum seurati and Phylum: Bryozoa 1.99  0.47 Absent
bryozoan sp. construction of artificial structures, but they are also the site of
Cladoceran sp. Order: Cladocera 0.004  0.001 Absent shipping and mariculture activities, renown vectors of alien species
Centropages brachiatus Subclass: Copepoda 0.05  0.01 0.0005  0.0003 (Glasby et al., 2007). Alien species recruit particularly well to con-
and Harpacticoida sp. crete surfaces in estuaries (Glasby et al., 2007), as supported
Cyclograpsus punctatus Order: Decapoda 2.22  1.56 Absent
Hymenosoma orbiculare Order: Decapoda 3.02  1.21 0.38  0.38
through our findings, and increased availability of hard substrata
Chironomus larvae Order: Diptera 8.35  0.8 0.72  0.22 clearly plays an important role in facilitating rapid expansion of
Chironomus pupae Order: Diptera 0.12  0.02 Absent F. enigmaticus. Schwindt et al. (2004b) recorded a very large in-
Tomichia ventricosa Class: Gastropoda 172.97  31.5 Absent crease in F. enigmaticus biomass in the Mar Chiquita Lagoon linked
Nematode sp. Phylum: Nematoda 0.11  0.02 0.05  0.01
to increased dumping of cans and other trash into the system,
Ischnura senegalensis Order: Odonata 1.62  0.33 Absent
Paracypridinae sp. Class: Ostracoda 0.81  0.5 0.06  0.03 associated with water sports and fishing activities.
Sarscypridopsis sp. Class: Ostracoda 1.52  0.2 0.19  0.08 The rapid expansion of Ficopomatus enigmaticus had major im-
Ceratonereis Class: Polychaeta Absent 0.03  0.01 pacts on other elements of the fauna, as this species plays an
Ficopomatus enigmaticus Class: Polychaeta 8050  6550 Absent important role as an ecosystem engineer. The reef it creates is
Total biomass 8279.104 1.9505
complex and creates a highly heterogeneous environment. Invasive
 K.A. McQuaid, C.L. Griffiths / Estuarine, Coastal and Shelf Science 138 (2014) 101e106 105

Fig. 2. Maps of various stages of physical manipulation to Zandvlei showing hardening of the banks. Solid lines represent concrete walls and dotted lines represent sand.

species that physically modify the environment have cascading
impacts on associated fauna and flora and therefore greatly affect
invaded ecosystems (Crooks, 2002; Wallentinus and Nyberg, 2007).
Introduced species that create habitat generally increase the
abundance and species richness of associated assemblages, while
those that decrease habitat complexity, by destroying structure,
tend to decrease abundance and richness. For example, in California
the exotic mussel Musculista senhousia constructs byssal mats on
soft sediments, facilitating great increases in the density of mac-
rofaunal organisms and species richness (Crooks, 1998). In south-
eastern Australia, the invasive alga Caulerpa taxifolia also in-
troduces complexity into areas lacking structure and has a positive
effect on a native clam species, Anadara trapezia, through the pro-
vision of shelter (Byers et al., 2010). It is important to note that the
impact of habitat-forming invasives on native communities is
highly complex, and can include both positive and negative effects
(Gribben et al., 2013). The role of marine invasive species as
ecosystem engineers has received limited attention and this study
therefore offers a valuable and quantitative example of the major
changes that can be brought about by invasive engineers.
In the Zandvlei the key change has been a transformation from
sandy banks to concrete walls, followed by progressive colonisation
of these walls by Ficopomatus enigmaticus reef. In a historical
context we thus see the progressive construction of concrete walls
around the Zandvlei, reducing habitat availability for sand-dwelling
and burrowing invertebrates, as the gentle, sloping banks were
transformed to steep, vertical walls, suitable for attached epifauna.
Estimations of the amount of soft and hard substrata, based on
historical maps (Fig. 2), show a change from 0 m of hard substratum
in 1942 to nearly 12 000 m in 2012. As hard substrata became
available, the population of F. enigmaticus established and then
proliferated, which in turn greatly affected the invertebrate com-
munity, since the habitat created by F. enigmaticus reef is far more
complex and heterogeneous than the soft sand originally found on
the banks of Zandvlei, or indeed bare concrete wall. In 2012, in
areas where the banks were in their original sandy condition, the
mean invertebrate biomass was only 2.0 g m2  1.77 SD, compared
to 7959.1  6481.10 g m2 where F. enigmaticus was present. Of this,
associated infauna living within the Ficopomatus reef comprised
229.1 g m2  262.53 SD. There has been an estimated increase in
the invertebrate biomass from only 0.30 t in 1942 to 14.33 t in 1986,
several years after the marina was developed, to 56.80 t in 2012e
an increase of almost 200 fold.
Not only did invertebrate biomass increase from sand to reef
habitat, but there was also a significant positive correlation be-
tween reef mass and infaunal biomass, density and number of
species. Greater reef biomass was associated with increased
abundance and biomass of infauna, as well as a greater number of
infaunal species. This is because, as reef mass increases, the habitat
becomes more complex and heterogeneous, increasing the avail-
ability of shelter and feeding sites and therefore enhancing species
richness (Bell and Galzin, 1984). This supports other studies
showing that the effects of habitat-forming invasives are biomass
dependent. Coral reef cover has been shown to have a positive
relationship with reef fish, with the total number of fish species and
individuals increasing as reef cover increases (Bell and Galzin,

Table 3
Length of concrete wall and sand bank in Zandvlei in 1942, 1986 and 2012 with estimated invertebrate biomass, including F. enigmaticus.

Year Length of wall Mean vertical reef Mean invertebrate Total biomass Length of sand Mean distance Mean invertebrate Total biomass Total in system (t)
covered in height (m)  SD biomass (g m2)  SD on reef (t) bank (m) to 0.6 m depth biomass (g m2)  SD on sand (t)
reef (m) (m)  SD

1942 0 0 0 0 7000 21.1  13.36 2.0  1.77 0.3 0.3

1986 8468 0.6  0.25 2776.7a 14.12 5354 21.1  13.36 2.0  1.77 0.23 14.33
2012 11 846 0.6  0.25 7959.1  6481.10 56.57 5354 21.1  13.36 2.0  1.77 0.23 56.80
a
Calculated by extrapolating values from 2012 and therefore no standard deviation.
106 K.A. McQuaid, C.L. Griffiths / Estuarine, Coastal and Shelf Science 138 (2014) 101e106
1984). In Australia the biomass of the invasive alga Caulerpa taxi-
folia was also positively correlated with the abundance and species
richness of the epifaunal community, while it was negatively
correlated with the abundance of associated infaunal soft-sand
communities (Gribben et al., 2013).
In terms of species richness, 16 invertebrate species were asso-
ciated with Ficopomatus enigmaticus reefs, compared to only 10
found in the sand. Taxonomic differences included a greater number
of epifaunal and sedentary species, such as the snail Tomichia ven-
tricosa and two bryozoan species, associated with reef rather than
sand. The crab Cyclograpsus punctatus was also absent from sand and
Hymenosoma orbiculare was found in greater abundance in the reef,
where it is provided with protection from predators. This supports
the findings of Schwindt et al. (2001), who showed a greater abun-
dance of crabs associated with F. enigmaticus reef than non reef areas.
There were no strong trends in taxonomic structure with changing
reef mass; however T. ventricosa, the two bryozoan species and
Chironomus larvae all showed a positive correlation with reef mass.
Ficopomatus enigmaticus can clearly have major impacts on native
biodiversity and precautionary measures should be taken to prevent
or decrease the spread of this highly invasive alien species. Recrea-
tional vessels should be cleaned before being transported between
estuaries, as this is a likely vector for F. enigmaticus infestation, and
care should be taken in the engineering of estuaries to minimise the
use of concrete walls and other artificial structures. Dumping of hard
objects, such as cans, rocks and tree trunks should also be avoided, so
as to limit the availability of suitable substrata. By limiting the amount
of hard substrata in an estuary, the risk of invasion by F. enigmaticus
and other similar alien invertebrates can be greatly decreased.
Further research is required to understand the ecological im-
pacts of Ficopomatus enigmaticus invasions, for example in terms of
the ability of an invaded system to support bird and fish assem-
blages, the role that the filter-feeding activities of F. enigmaticus
play in water quality and the potential impacts of removing reef
mass from a system.
Acknowledgements
We thank the Postgraduate Funding Office of the University of
Cape Town, the Marine Research Institute of the University of Cape
Town, the DST-NRF Centre of Excellence for Invasion Biology and
the South African National Research Foundation for funding. Joshua
Gericke and Vera Liebau kindly helped in the field and Tadeusz
Namiotko and Wayne Florence assisted in identifying infaunal
species.
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