epibiotic traits of the invasive red seaweed acanthophora spicifera in la paz bay, south baja...

ORIGINAL ARTICLE

Epibiotic traits of the invasive red seaweed Acanthophoraspicifera in La Paz Bay, South Baja California (EasternPacific)Enrique Avila1,2, Marıa del Carmen Mendez-Trejo2,3, Rafael Riosmena-Rodrıguez2,Juan M. Lopez-Vivas2 & Abel Sentıes3

1 Instituto de Ciencias del Mar y Limnologıa, Estacion El Carmen, Universidad Nacional Autonoma de Mexico, Ciudad del Carmen, Campeche,

Mexico

2 Programa de Investigacion en Botanica Marina, Departamento de Biologıa Marina, Universidad Autonoma de Baja California Sur, La Paz, Baja

California Sur, Mexico

3 Departamento de Hidrobiologıa, Universidad Autonoma Metropolitana–Iztapalapa, Mexico

Introduction

Introduced seaweed species are capable of profoundly

altering host ecosystems by impacts on biodiversity, habi-

tat modification, effects on fish and invertebrate fauna,

toxic effects on other biota and alterations in competitive

relationships (Schaffelke & Hewitt 2007). Similar to ter-

restrial invasive plants, seaweeds can outcompete native

species for resources such as nutrients, light and physical

space. Also, exotic seaweeds may become successful in the

Keywords

Acanthophora spicifera; epiphytism; epizoism;

invasive species; Mexican Pacific; sponge

assemblages.

Correspondence

Enrique Avila, Instituto de Ciencias del Mar y

Limnologıa, Estacion El Carmen, Universidad

Nacional Autonoma de Mexico, Carretera

Carmen-Puerto Real km. 9.5, Ciudad del

Carmen, Campeche, C.P. 24157, Mexico.

E-mail: [email protected]

Accepted: 20 January 2012

doi:10.1111/j.1439-0485.2012.00511.x

Abstract

The aim of this study was to analyze the interaction of a non-native macroalga

(Acanthophora spicifera) with native macroalgae (Sargassum spp.) and sponge

assemblages in a subtropical embayment of the Mexican Pacific. The intensity

of A. spicifera epiphytism on the native seaweed Sargassum varied significantly

over time and was inversely related to the Sargassum density and size. The

higher intensity (up to 28 individuals per host plant) occurred when Sargassum

was smaller and was lower in density (senescence period). The lower intensity

was recorded during the growth period of Sargassum and the subsequent

increase in intensity was attributed to a high fragmentation period of A. spicifera,

which was evidenced by a decrease in its average size and biomass and by the

presence of larger free-floating accumulations on the subtidal zone. The facul-

tative interaction between A. spicifera and Sargassum appears to be neutral, as

no negative or positive effects were found for epiphytic or basibiont seaweeds.

However, this invasive seaweed characteristically monopolizes almost all types

of hard substrate, and its effects on other algae and benthic organisms should

be investigated. Moreover, A. spicifera was often epizoic on epilithic sponges.

This invasive seaweed was found anchored on the sponge tissue by rhizome-

like structures. In addition, free-floating fronds of A. spicifera were frequently

found carrying small pieces of the basibiont sponge in its basis (60% of them

with eggs and embryos), which suggests a novel facilitation mechanism for

some sponge species, as the A. spicifera epizoism could favor fragmentation,

dispersal and recruitment of these invertebrates. This study shows that A. spicifer-

a is not only a species that adapts rapidly to the new conditions of the receiv-

ing environment but, due to its epibiotic traits, it can directly interact with

and influence the life histories of some native species.

Marine Ecology. ISSN 0173-9565

Marine Ecology (2012) 1–11 ª 2012 Blackwell Verlag GmbH 1

new environment because of their reproductive traits,

rapid spread and capabilities to overgrow a wide variety

of inert and live substrata. For example, the red seaweed

Dasya sessilis Yamada is restricted in the Mediterranean

to rocky and hard substrata, but in Galician coasts (where

it was recently introduced) it is epizoic on Mytilus and

Balanus as well as epiphytic on maerl beds (Pena & Bar-

bara 2006). The Asian green alga Ulva pertusa Kjellman

has been described in the Pacific coasts of Baja California

(Mexico) as epiphytic on a wide variety of algae and epi-

zoic on mussels (Aguilar-Rosas et al. 2008). However,

although the epibiotic traits seem to be common in many

invasive seaweed species, there has been little documenta-

tion of the kinds of interaction with and the effects on

the basibiont species (Davis et al. 1997; Baldacconi &

Corriero 2009).

The red seaweed Acanthophora spicifera (M. Vahl)

Børgesen (Rhodophyta: Rhodomelaceae), native to Florida

and Caribbean, currently has a nearly continuous distri-

bution in all tropical and subtropical seas of the world

(Global Invasive Species Database 2010). However, there

has been little investigation of the impacts of this species

beyond its native range. In Hawaii, for example, A. spicif-

era has been regarded as the most widespread and inva-

sive alien macroalga after being unintentionally

introduced in early 1950s (Doty 1961; Russell 1992). The

main impact reported from this seaweed is space mono-

polization; the large biomass of this species affects (by

smothering and outcompeting) a wide range of native

flora and fauna (Russell & Balazs 1994; Eldredge 2003;

O’Doherty & Sherwood 2007; Tsuda et al. 2008). It has

also been suggested that the success of this species in

invading new habitats is due to its high morphological

plasticity, reproductive strategies (both sexually and asex-

ually), adaptability to a wide range of hydrological condi-

tions as well as its successful epiphytism on other algae

(Russell 1992; Smith et al. 2002). In the eastern tropical

Pacific, blooms of A. spicifera covered by cyanobacterial

epiphytes have been observed at several reefs and were

associated with a widespread coral mortality during the

1997–1998 El Nino Southern Oscillation (Fong et al.

2006).

Recently, a new population of this species has been

detected on the Pacific coasts of Mexico, particularly in La

Paz Bay (Southwestern Gulf of California). This seaweed

was seen for first time in the summer of 2006, covering a

small area near of the Port of Pichilingue (R. Riosmena-

Rodrıguez unpublished data). Nevertheless, it is now

widely distributed throughout the shallow rocky shores

southeast of La Paz Bay. These areas have been dominated

by Sargassum spp., one of the most important species (for

biodiversity) of this region, and according to preliminary

observations, A. spicifera is now an epiphyte of this algae

and various invertebrates. However, until now there have

been no studies focused on the dynamics and potential

effects of this invasive species on native biota.

This study therefore aims to analyze: (i) the effects of

A. spicifera epiphytism on the native seaweed Sargassum

spp. Setchell and Gardner and its spatial and temporal

variation; (ii) whether a relationship exists between the

intensity of epiphytism by A. spicifera and the seasonal

variations on Sargassum density and size and the water

temperature; and (iii) the potential effects of this invasive

seaweed on local sponge assemblages. In addition, the

occurrence of facilitative interactions between A. spicifera

and sponge assemblages is also discussed.

Material and Methods

Study area

The study area was in La Paz Bay, a coastal lagoon

located in the Southwestern Gulf of California (between

24�12¢07¢¢ N and 110�17¢59¢¢ W) in Northwestern Mexico

(Fig. 1). This is the largest (80 km long and 35 km wide)

and deepest (down to 450 m) coastal lagoon in the Gulf

of California (Obeso-Nieblas et al. 2008). The region has

a dry and arid climate of type BW (h’) hw (e’) with two

contrasting seasons each year, the dry season (from Octo-

ber to June) and the rainy season (from July to Septem-

ber). The average annual rainfall is 200 mm with a mean

annual air temperature of 24 �C (Kottek et al. 2006; Con-

treras 2010). In La Paz Bay the tidal regime is semidiurnal

and salinities range between 34 and 36 depending on the

time of year (Jimenez-Illescas et al. 1997). The sea surface

temperature ranges from 18 �C in winter to 28 �C in

summer (Arreola 1991).

This study was carried out at Punta Roca Caimancito

(24�12¢22¢¢ N–110�18¢02¢¢ W) in the southeast coast of

this bay and about 6 km from the commercial Port of

Pichilingue. At this locality, three sampling sites (�500 m

apart) were selected in the subtidal zone (1–5 m depth),

which are representative of the bottom type on the bay:

(1) a predominantly rocky zone with a high mussel abun-

dance; (2) a rocky zone interspersed with patches of sand;

(3) a rocky zone dominated by the massive coral Porites

panamensis Verrill. In the three sites, A. spicifera has

become the dominant seaweed species, forming dense

beds and covering almost all types of hard substrata.

Environmental parameters

The environmental parameter recorded during the study

period (from April to September 2010) was the water

temperature (�C). The average monthly temperature

was determined from daily measures at 12:00 h with a

Epibiotic traits of Acanthophora spicifera Avila, Mendez-Trejo, Riosmena-Rodrıguez, Lopez-Vivas & Sentıes

2 Marine Ecology (2012) 1–11 ª 2012 Blackwell Verlag GmbH

temperature sensor (HOBO data logger), which was

permanently placed at 2 m depth on the seafloor.

Substratum types inhabited by Acanthophora spicifera in La

Paz Bay

To determine the substratum types A. spicifera inhabits,

four 100-m lineal transects were placed running perpen-

dicular to the shore (1–6 m depth) within the study area.

Each transect was separated by a distance of 50 m. The

relative proportion (%) of the substratum types A. spicif-

era inhabits was determined in 10 quadrats, 1 · 1 m

(divided into grids of 10 · 10 cm), which were randomly

placed along each transect (40 m2 in total). The areas

covered by sand within the quadrats and the cases of epi-

phytism on other seaweeds were not considered in this

determination. Sandy patches were excluded because, in

accordance with preliminary observations, this seaweed

inhabits only hard substrata and we wished to represent

the relative percentage of substrata colonized by this alga.

The epiphytism on other algae was analyzed by a different

method (see below).

Determination of biomass and size of Acanthophora

spicifera

The biomass of A. spicifera was determined monthly

(from April to September 2010) in the three sampling

sites. In each site, nine quadrats (5 · 5 cm) were placed

randomly within the A. spicifera distribution range. In

each quadrat, all individuals of this species were cut off

from their holdfast and immediately placed in plastic

bags. The total area sampled in each site was 0.0225 m2.

In the laboratory, samples were dried in a stove (at 60 �C

for 24 h) and weighed (g). Then, the biomass was

expressed as gÆDWÆm)2. The average size (cm) of plants

was also obtained in the same samples, but before drying

them.

Epiphytism by Acanthophora spicifera on Sargassum spp.

and epizoism on sponges

According to preliminary observations, A. spicifera may

overgrow invertebrates and be epiphytes of other sea-

weeds. In this study, the intensity of A. spicifera epiphyt-

ism on the native macroalgae Sargassum spp. (the

dominant perennial seaweed in the subtidal zone until

the A. spicifera invasion) and the epizoism on sponges

has been examined. To assess the epiphytism on Sargas-

sum, at each site, three 0.25 · 0.25 m2 quadrats were ran-

domly placed and all the Sargassum plants within the

quadrant were completely cut off below their holdfasts by

SCUBA divers. The algae were immediately placed in

plastic bags and transported to the laboratory. For each

site, the total sampled area was 0.18 m2. In the labora-

tory, all the Sargassum thalli were quantified for abun-

dance determinations (indÆm)2) and the length measured

(cm) from the holdfast to the apex of the longest frond.

The intensity of A. spicifera epiphytism was determined

by counting the number of individuals of Acanthophora

per Sargassum plant. These determinations were made at

monthly intervals from April to September 2010.

Sponges overgrown by A. spicifera, as well as free-living

fragments of macroalga-carrying sponges, were commonly

seen in the study area. Therefore these interactions were

briefly described. The abundance of the free-living inter-

actions (A. spicifera per sponge) was assessed in three

transects (20 m long · 2 m wide), which were placed

perpendicular to the shore in each site. In each transect,

all the free-living fragments of A. spicifera-containing

sponges were counted and collected. The total area sam-

pled in each site was 120 m)2. In the laboratory, sponges

were identified and the relative frequency (%) of each

Fig. 1. Map of the study area showing the location of the sampling

sites at La Paz Bay, Baja California Sur, Mexico.

Avila, Mendez-Trejo, Riosmena-Rodrıguez, Lopez-Vivas & Sentıes Epibiotic traits of Acanthophora spicifera


species was recorded. To determine whether the size of

sponge fragment is a function of the size of A. spicifera

fragment, the specimens (sponge and alga) were separated

and their volume (ml) was determined by displacement

in water, using a graduated cylinder.

Data analysis

To test whether the intensity of A. spicifera epiphytism

and the biomass and size of this seaweed varied over the

time (6 months) and among sites (three sites), one-way

repeated-measures analyses of variance (ANOVA) were

performed (time and site were random factors), followed

by the post-hoc analysis by the Student–Newman–Keuls

(SNK) test (Underwood 1997). To verify normality and

homogeneity of variances, the Kolmogorov–Smirnov and

Bartlett tests were used. Only biomass data required

square root-transformation to satisfy assumptions for an

analysis of variance. One-way ANOVA followed by the

SNK test was also used to compare the frequency of free-

living sponge ⁄ A. spicifera associations between the three

sites assessed. Spearman’s rank correlation coefficients

were used to test whether a relationship exists between

(1) the intensity of A. spicifera epiphytism and the water

temperature and population descriptors of Sargassum

(density and size) and (2) the volume of sponge frag-

ments and those of the drifting A. spicifera fragments.

Results

Water temperature and substratum types

Monthly average water temperature showed a temporal

fluctuation with the highest values in September

(29.2 ± 0.16 �C) and the lowest in April (23.5 ± 0.12 �C).

The maximum value (30.9 �C) was recorded in Septem-

ber and the minimum (20.5 �C) in May.

The main substratum types inhabited by A. spicifera in

the study area were: rocky (48.5 ± 4.9%), mussels (45.6 ±

0.4%) (Fig. 2A), sponges (4.9 ± 3.1%) (Fig. 2B) and coral

A B

C D

E FFig. 2. (A) Acanthophora spicifera overgrow-

ing mussels (Modiolus capax), (B) sponges

(Tedania sp.) and (C) corals (Pocillophora sp.).

(D) Drifting frond of A. spicifera carrying a

sponge fragment (Callyspongia californica). (E)

Root-like structure of A. spicifera developed to

attach on sponges. (F) Brood chamber contain-

ing eggs and embryos in a sponge fragment

(Haliclona turquoisia) attached to a drifting

frond of A. spicifera.



rubble (1.0 ± 1.4%). A smaller proportion was found

attached to shells and gravel. At the site dominated by

corals, this seaweed was occasionally seen overgrowing

some live corals (Fig. 2C) (Pocillopora sp. and Porites pan-

amensis Verrill), but its frequency was not quantified.

Biomass and size of Acanthophora spicifera

According to the repeated measures ANOVA, the average

biomass and size of A. spicifera showed significant (bio-

mass: df = 5, F = 5.81, P < 0.01; size: df = 5, F = 5.66,

P < 0.01) changes during the study period. From April to

August the average biomass showed a significant decrease

from 1069.3 ± 57.8 to 832.7 ± 43.7 gÆDWÆm)2. Then, a

new increase in biomass was detected from August to

September to 1178.7 ± 87.7 gÆDWÆm)2 (Fig. 3). A similar

pattern was recorded in the average size, the largest sizes

being recorded in the April–May period (11.2 ±

0.19 cm), followed by a decrease until August (8.6 ± 0.28

cm). Then, from August to September an increase was

observed (10.6 ± 0.25 cm) (Fig. 3).

Both variables also showed significant differences

among sites (repeated measures ANOVA, biomass:

df = 2, F = 19.91, P < 0.01; size: df = 2, F = 7.59, P <

0.01). The average biomass and size of A. spicifera was

generally higher in site 1 (predominantly rocky zone with

a high mussel abundance) than in the other two sites.

Epiphytism on Sargassum spp.

The host seaweed Sargassum showed a growth period

from spring to early summer, which was followed by a

senescence period (fragmentation) from May to Septem-

ber. The highest average (±SE) size was in April

(31.8 ± 1.5 cm) and the lowest in July (10.4 ± 0.3 cm)

(Fig. 4A). The smaller sizes (<15 cm) found from July to

September corresponded to the basal holdfast portion and

stipes. The Sargassum density was higher between May

and June (213 ± 45.3 and 208 ± 45.3 indÆm)2, respec-

tively) and then decreased until September (53 ± 7.5

indÆm)2) (Fig. 4A).

The Acanthophora spicifera epiphytism occurred

mainly on the lower portions (<15 cm) of the Sargas-

sum thalli (holdfast and stipe) and its intensity varied

significantly (repeated measures ANOVA, df = 5, F =

40.38, P < 0.05) over time but not among sites

(repeated measures ANOVA, df = 2, F = 1.84, P > 0.05).

The lower intensities were recorded from April to June

(fewer than five individuals of A. spicifera per Sargassum

plant). Then, in the July–August period the intensity

increased to up to 28 individuals per host plant. From

August to September a new decrease in the A. spicifera

epiphytism was detected (18.8 ± 0.6 individuals per host

plant) (Fig. 4B). The intensity of A. spicifera epiphytism

covaried negatively with size (Spearman’s r = )1.0,

P < 0.01) of Sargassum, showing that the epiphytism

was lower when the host was longer than 15 cm. Also,

a similar inverse tendency, although not significant, was

observed between the intensity of A. spicifera epiphytism

and Sargassum density (Spearman’s r = )0.6, P > 0.05),

indicating that epiphytism was higher at densities lower

than 100 Sargassum thalli m)2 (Fig. 5). There was no

significant correlation between the intensity of epiphyt-

ism and the water temperature, although the period of

higher intensity did coincide with warmer temperatures

(24–30 �C).

Acanthophora spicifera epizoism on sponge assemblages

The A. spicifera epizoism on sponges occurred mainly in

epilithic species with massive and cushion-shaped growth

forms (Table 1). In this interaction, sponges are not epi-

phytes of A. spicifera, as often occurs in other sponge–sea-

weed associations, but rather free-living fragments of this

alga entangle the surface of these invertebrates and then

overgrow it almost completely (Fig. 2B). Cross-section

analyses revealed that A. spicifera develops rhizomatous

holdfasts (Fig. 2E) that penetrate the sponge tissue to a

depth of 1–3 cm, whereas on hard substrata (e.g. mollusk

shells, coral ruble and other seaweeds) it forms irregularly

lobed discs.

A total of 44 free-living fragments of A. spicifera were

collected containing sponge fragments (seven species

belonging to five families). The most abundant sponges

were Haliclona turquoisia de Laubenfels (mean fre-

quency = 43.6 ± 10.1%), Callyspongia californica Dickinson

(25.7 ± 17.2%) (Fig. 2D) and Lissodendoryx (Waldoschmit-

tia) schmidti Ridley (19 ± 11.7%). The frequency was

Fig. 3. Monthly average biomass (shaded bars, primary axis) and size

(line, secondary axis) of Acanthophora spicifera at Punta Roca Cai-

mancito in La Paz Bay.



lower than 10% in the species Haliclona caerulea Hechtel,

Mycale ramulosa Carballo and Cruz-Barraza, Dysidea sp.

and Haliclona sp. (Table 1). The average volume of

sponge fragments (3.7 ± 0.9 ml) was in general lower

than that of the free-floating fronds of A. spicifera

(6.8 ± 1.9 ml) (Table 1). Interestingly, 60% of the sponge

fragments (e.g. in M. ramulosa, Dysidea sp. and H. tur-

quoisia) collected had brood chambers containing eggs

and embryos (Fig. 2F). Other sponge species such as Geo-

dia media Bowerbank, Chondrilla nucula Schmidt, Teda-

nia sp. (Fig. 2B) and Hyatella intestinalis Lamarck were

also observed overgrown by this alga, but fragments of

these species were never found attached to drifting frag-

ments of A. spicifera.

A significant positive relationship (Spearman’s r = 0.6,

P < 0.01) was found between the volume of sponge frag-

ments and the volume of the A. spicifera fragments

(Fig. 6, Table 1), showing that the size of sponge frag-

ments is a function of the size of A. spicifera fragment.

Moreover, one-way ANOVA indicated that there were

significant differences in the percentage of frequency of

free-living sponge ⁄ A. spicifera interactions between sites

(P < 0.01). The frequency was significantly higher (SNK

test, P < 0.01) in site 3 (rocky with coral patches) than in

the other two sites.

Discussion

The introduction of Acanthophora spicifera to the Gulf of

California is relatively recent. It was observed for the first

A

B

Fig. 4. (A) Monthly average density (shaded bars, primary axis) and

size (line, secondary axis) of Sargassum spp. during the study period.

The average values of density and size are from the three sites. (B)

Number of individuals of A. spicifera per Sargassum plant. The error

bars show the standard error.

Fig. 5. Inverse relationships between the Acanthophora spicifera epi-

phytism and the average size (discontinuous line, black circles) and

density (continuous line, white triangles) of Sargassum in Punta Roca

Caimancito.

Table 1. Sponge species found in association with Acanthophora spi-

cifera in Punta Roca Caimancito. The table also shows the relative fre-

quency (%) of the sponge species found attached to drifting

fragments of A. spicifera in the three sampling sites (site 1 = predomi-

nantly rocky zone, site 2 = rocky zone with patches of sand and site

3 = rocky zone with coral patches), their growth forms (M = massive,

A = arborescent, C = cushion shape, R = repent, F = fistulose, E =

encrusting) and the average volume of free-living fragments of

sponges and A. spicifera.

Sponge

species

Growth

form

Frequency (%)

Fragment volume

(mean ± SE)

Site

1

Site

2

Site

3 Sponge A. spicifera

L. (W.) schmidti M 28.6 28.6 n.d. 3.4 ± 2.0 5.2 ± 3.4

M. ramulosa A n.d. n.d. 3.2 18 ± 0.0 2 ± 0.0

C. californica C 28.6 n.d. 48.4 3.4 ± 1.8 5.7 ± 4.2

H. turquoisia R 28.6 57.1 45.2 2.1 ± 0.5 4.4 ± 1.1

H. caerulea M n.d. n.d. 3.2 20 ± 0.0 20 ± 0.0

Haliclona sp. C 14.3 n.d. n.d. 20 ± 0.0 40 ± 0.0

Dysidea sp. M n.d. 28.6 n.d. 13 ± 2.8 60 ± 56.6

Tedania sp.* F

Geodia media* M

Chondrilla

nucula*

E

Hyatella

intestinalis*

M

The asterisk indicates the species that were also found fouled by the

invasive seaweed but free-living fragments of these species were

never found. n.d. = not determined.



time in summer 2006 covering a small area in the locality

of Costa Baja, near to the Port of Pichilingue at La Paz

Bay (unpublished data). It has since spread through pro-

tected rocky shores of the southeastern of this bay and is

now a common component of the subtidal community.

Although how it was introduced remains unknown, an

unintentional introduction through fouling on cruisers

could be possible. Some of these ships make several trips

during the year from Florida to San Diego (USA) cross-

ing the Panama Canal, and one of the ports of call is the

Port of Pichilingue within La Paz Bay. So it is probable

that this seaweed has been transported by these vessels

from the Caribbean or from the Pacific coasts of Central

America, where it has also been described recently (Pan-

ama: Glynn et al. 2001; Fong et al. 2006; Costa Rica:

Cortes 2001 and El Salvador: Molina 2004). The intro-

duction of this seaweed via fouling on vessels has been

suggested in other locations of the Central Pacific such as

Guam, Marshall Islands and Hawaii (Doty 1961; Tsuda

et al. 2008). However, to confirm the origin of these pop-

ulations, phylogeographyc studies are required.

One of the most evident effects of its introduction to

La Paz Bay is substratum monopolization, as this invasive

seaweed forms dense beds colonizing almost all types of

hard substrata (from the intertidal to 5–6 m depth).

Although the potential effects of space monopolization

were not analyzed in this work, it generally has detrimen-

tal effects on native communities. These effects may be

related to competition for resources (e.g. nutrients and

available substrata) with other seaweeds, smothering and

reduction in abundance ⁄ biomass of sessile organisms as

well as changes in species composition (see review by

Schaffelke & Hewitt 2007; Bulleri et al. 2010). These inva-

sive traits are consistent with those documented in

Hawaii, where high biomass of this species affects (by

smothering and outcompeting) a wide range of native

flora and fauna (Russell & Balazs 1994; Eldredge 2003;

O’Doherty & Sherwood 2007; Tsuda et al. 2008). On the

Pacific coasts of Central America, A. spicifera (living in

association with cyanobacterial symbionts) has been

described as a successful opportunistic species in coral

communities after a widespread coral mortality during

the 1997–1998 El Nino Southern Oscillation (Fong et al.

2006). Moreover, it has been documented that the high

densities of A. spicifera have a negative effect on native

seaweed species by reducing the light conditions and

nutrients available to them (Sanchez et al. 2005; Wallenti-

nus & Nyberg 2007).

Acanthophora spicifera epiphytism on Sargassum spp.

The intensity of A. spicifera epiphytism was inversely cor-

related with Sargassum size and density, i.e. the high

intensity occurs when the basibiont plant was smaller

(<15 cm) and with a lower density (<100 thalliÆm)2).

This result could be contradictory if considering the

hypothesis that more complex habitats generally also have

a greater surface area to support a larger number of spe-

cies and abundance (Hauser et al. 2006). However, simi-

lar inverse relationships have been documented between

other Sargassum species [e.g. Sargassum natans (Linnaeus)

Gaillon, Sargassum muticum (Yendo) Fensholt, Sargassum

cymosum C. Agardh and Sargassum spp.] and its epiphytic

flora and fauna (Conover & Sieburth 1964; Withers et al.

1975; Jephson & Gray 1977; Leite & Turra 2003; Avila

et al. 2010). The negative relationship between the

S. cymosum biomass and the Hypnea musciformis (Wul-

fen) Lamouroux epiphytism (from Lamberto’s Beach,

Brazil) was attributed to a possible effect of the epiphytic

algae on the growth and survival of the macroalgae sub-

stratum (Leite & Turra 2003), as epiphytes may reduce

the photosynthetic rates of the basibiont macroalgae and

increase branch fragmentation (Buschmann & Gomez

1993). In S. natans and S. muticum it was suggested that

these species can reduce the epiphyte load by means of

production of tannin-like substances during their growth

stage (Conover & Sieburth 1964; Withers et al. 1975;

Jephson & Gray 1977). These substances inhibit the devel-

opment of surface microflora, which is considered a nec-

essary prerequisite for the settlement of epiphytic

organisms (Martınez-Nadal et al. 1965; Ryland 1974) and

may be significant in determining the epibiont abundance

and species richness (Blight & Thompson 2008). In this

case, the intensity of epiphytism was not so heavy as to

Fig. 6. Positive relationship (r = 0.6, P < 0.01) between the volume

of the sponge fragments and the volume of Acanthophora spicifera

fragments.



have adverse effects on the host integrity, but it is

unknown whether the epiphytism by A. spicifera can be

regulated by polyphenolic compounds.

On the other hand, the period of higher intensity of epi-

phytism (June–August) also coincided with a period of high

fragmentation ⁄ dislodgement of A. spicifera (E. Avila, per-

sonal observations), which could be related to the decrease

in the average biomass and size of this exotic seaweed in

this same period. So an increase in drifting fragments pro-

duction in the water column may increase the chance to

snagging and attaching on these larger seaweeds. Further-

more, the high specificity of A. spicifera to the lower por-

tions (holdfast and stipes) of Sargassum was likely because

these parts remain after the seasonal fragmentation of this

perennial plant (May–July) (Avila et al. 2010), and because

there is less movement in comparison with the distal parts,

which is required for fragments to snag (Kilar & McLachlan

1986). This capability of A. spicifera to snag and attach to

fronds of other seaweed species [e.g. Hypnea musciformis

(Wulfen) Lamouroux, Laurencia nidifica J. Agardh, Palis-

ada perforata (Bory de Saint Vicent) K.W. Nam (as Lauren-

cia papillosa)] has been documented previously (Kilar &

McLachlan 1986; Russell 1992). In fact, it has been sug-

gested that A. spicifera benefits from this association by

being shielded from sunlight, and being somewhat pro-

tected from desiccation during low tides (Russell 1992).

At La Paz Bay, the facultative relationship between

A. spicifera and Sargassum seems to be a product of the

continuous drifting fragment production and to the high

snagging capabilities of A. spicifera. Although in this inter-

action there was no direct evidence of negative effects on

these native seaweeds, the potential impact of space

monopolization that produces A. spicifera on other mem-

bers of the community needs to be investigated. It is possi-

ble that the effects of this invasion on Sargassum beds were

not evident because of the relatively large size (up to 50 cm

high) of this seaweed. However, to avoid generalizations, it

is necessary to evaluate the impacts on a representative set

of the whole community of seaweeds and benthic organ-

isms of the study area. As was commented previously, the

effects of space monopolization by invasive seaweeds can

cause smothering and losses in abundance ⁄ biomass and

available substrate for recruitment of other organisms

(Eldredge 2003; Baldacconi & Corriero 2009; Bulleri et al.

2010). At the moment, A. spicifera has a distribution

throughout shallow rocky shores southeast of La Paz Bay,

but the possibility that this seaweed extends and invades

other areas of the Gulf of California is not discarded.

Acanthophora spicifera epizoism on sponge assemblages

The effects of alien macroalgae on local sponge assem-

blages have scarcely been investigated. For example, the

introduced green algae Caulerpa scalpelliformis (R. Brown

ex Turner) C. Agardh in Botany Bay (New South Wales;

Davis et al. 1997) and Caulerpa racemosa var. cylindracea

(Sonder) Verlaque, Huisman et Boudouresque in the

Apulian coast (Ionian Sea, Italy; Baldacconi & Corriero

2009) are some of the few described alien species that

overgrow sponges. The introduction of both species has

caused a decline in the sponge coverage and, in the case

of C. racemosa, also a slight decline in the sponge species

richness (Davis et al. 1997; Baldacconi & Corriero 2009).

In this study, A. spicifera was often found overgrowing

epilithic sponge species (mainly those with massive and

cushion-shape growth forms) in the subtidal zone.

Although a negative impact on these invertebrates was

not evident, a likely effect on its filter-feeding efficiency is

not discarded. In the case of C. racemosa and C. scalpelli-

formis it was suggested that the sediment trapped by the

algal stolons may affect sponge pumping activity, produc-

ing a shift to a less diverse, more silt-tolerant assemblage

(Carballo et al. 1996; Davis et al. 1997; Baldacconi & Cor-

riero 2009).

Moreover, field observations and cross-section analyses

showed that A. spicifera develop rhizomatous holdfasts

that penetrate (1–3 cm) and anchor in the sponge tissue,

suggesting these invertebrates are used as substratum by

A. spicifera. Similar findings were documented in C. race-

mosa, which is anchored to the sponges through numer-

ous rhizoidal pillars that penetrate the sponge tissue to a

depth of several millimeters (Baldacconi & Corriero

2009). These rhizome-like structures developed by A. spi-

cifera were found only in association with sponges. In

harder substrata such as coral rubble, rocks, mussels and

other seaweeds, A. spicifera develops irregular lobed discs.

On the other hand, sponge fragments were often seen

attached to the basis of free-floating fronds of A. spicifera,

suggesting the algae could be a mean of transport and

dispersal for sponges. Previous studies have found that

rafting on floating seaweeds is a mechanism whereby

many intertidal animal species can be dispersed over long

distances, possibly hundreds of kilometers or more (Ing-

olfsson 1995).

Moreover, the significant positive relationship between

the volume of drifting fragments of the alga and those of

the sponges indicated that the sponge fragment size is a

function of the detached frond size. A similar effect was

experimentally demonstrated in the mussels Mytilus cali-

fornianus Conrad and Mytilus edulis Linnaeus, which are

usually dragged and dislodged by algal epizoans (kelps) at

Tatoosh Island (Washington State, USA; Witman & Such-

anek 1984). In this case, a negative effect on mussel pop-

ulations was suggested, as mussels overgrown by kelp

encountered flow-induced forces that were two to six

times greater than flow forces on the mussels alone



(Witman & Suchanek 1984). Dayton (1973) showed that

plants (of only 10 cm length) of Postelsia attached to

M. californianus incurred sufficient resistance to flow to

dislodge the underlying mussel. Similar findings have also

been reported in exotic species, which can alter the

hydrodynamic regime experienced by other species. For

example, the slipper limpet Crepidula fornicata and the

alga Codium fragile can increase drag on the species to

which they are attached, increasing dislodgement (see

review in Crooks 2009). In this study, our findings also

suggest that epizoism by A. spicifera can increase the risk

of sponge dislodgement or fragmentation. However, this

effect could be advantageous for sponges, as it is one of

its main modes of reproduction.

In addition, the presence of reproductive elements in

the sponge fragments attached to drifting fragments of

A. spicifera suggests an additional advantage for sponge

dispersal. Maldonado & Uriz (1999) found developing

embryos in free-living fragments of the sponge Scopalina

lophyropoda Schmidt (from the Mediterranean Sea) and

they suggested that the dispersal capacity of sexually pro-

duced propagules could be maximized by the additional

dispersal of the asexual propagules. Nevertheless, consid-

ering the high fragmentation ⁄ dislodgement rates of

A. spicifera (even under low water movement conditions),

its high dispersal and its high capability to snag the sub-

strata (Kilar & McLachlan 1986), this could indicate a

novel facilitation mechanism for fragmentation, dispersal

and recruitment of the basibiont sponges. The facilitative

mechanisms resulting from epibiosis have also been

described on drifting fragments of the invasive species

Codium fragile in Nova Scotia (Mathieson et al. 2003).

Drifting populations of this seaweed may be a good vec-

tor for the introduction of their epibionts such as the fila-

mentous red alga Neasophonia harveyi and several other

epiphytes. Another example of this facilitative mechanism

(involving transport) has been documented in the sponge

Halichondria panicea, which may change their distribution

area within the Lesina Lagoon (at Apulia, Southern Adri-

atic Sea) using free-living fronds of the alga Valonia aeg-

agropila as a vector (Nonnis-Marzano et al. 2004).

According to Rodrıguez (2006) a novel facilitation

develops if an invasive species is functionally unique in

comparison with native resident species and hence pro-

vides a new exploitable resource that is utilized by native

species. This facilitative mechanism was more evident in

relatively more brittle sponges such as H. turquoisia and

C. californica than in species with a more resistant struc-

ture (e.g. G. media, H. intestinalis and C. nucula), on

which, despite having been observed fouled by A. spicifer-

a, free-living fragments of these species were never seen.

Undoubtedly, more studies are required on this alga ⁄sponge interaction, e.g. to assess the success rate (dispersal,

attachment and survival) of fragments of A. spicifera-con-

taining sponges. Moreover, our findings indicated that

the frequency of the free-living sponge ⁄ A. spicifera inter-

actions vary significantly between sites. The higher fre-

quency in site 3 was possibly due to the orientation of

sites with respect to prevailing current direction. A greater

accumulation of free-floating fragments of A. spicifera was

also observed in the subtidal zone of this site compared

with the other two sites.

In summary, A. spicifera is an invasive species that

overgrows seaweeds and invertebrates in the Southwestern

Gulf of California. These epibiotic traits reflect the high

capability of this seaweed to adapt to the new environ-

ment. Although there was no evidence of damage on the

basibiont alga, the intensity of epiphytism was strongly

related to the Sargassum dynamics. The highest intensity

of A. spicifera epiphytism coincided with a seasonal

decrease in the density and size of Sargassum as well as

with a period of high fragmentation in A. spicifera. More-

over, many epilithic sponge species were found overgrown

by A. spicifera. In this epizoic interaction, a novel facilita-

tion mechanism was suggested – A. spicifera epizoism

contributing to the fragmentation, dispersal and recruit-

ment of some sponge species. Both epiphytic and epizoic

traits described in A. spicifera seem to be products of its

continuous fragmentation ⁄ dislodgement and its ability to

snag different substrate types (Kilar & McLachlan 1986).

Nevertheless, it is clear that the introduction of this sea-

weed deserves further investigation and long-term moni-

toring programs to determine the potential effects on

other members of the benthic community and its proba-

ble routes of propagation through the Gulf of California

coasts. For instance, parallel studies with this are being

carried out to evaluate the effects of this invasion on the

diversity and abundance of epibenthic mesofauna and

seaweed assemblages.

Acknowledgements

We acknowledge the support of the Consejo Nacional de

Ciencia y Tecnologia ⁄ Secretaria de Medio Ambiente y

Recursos Naturales (CONACYT-SEMARNAT) fund (Con-

tract No. 23235). E. Avila also thanks CONACYT for the

financial support (Postdoctoral Grant) and Direccion de

Investigacion Interdisciplinaria y Posgrado (DIIP) of the

Universidad Autonoma de Baja California Sur for their

support and facilities.

References

Aguilar-Rosas R., Aguilar-Rosas L.E., Shimada S. (2008) First

record of Ulva pertusa Kjellman (Ulvales, Chlorophyta) in

the Pacific Coast of Mexico. Algae, 23, 201–207.



Arreola L.J.A. (1991) Larvas de peces en la Ensenada de La Paz,

BCS. BSc Dissertation, Universidad Autonoma de Baja Cali-

fornia Sur, La Paz: 94 pp.

Avila E., Blancas-Gallangos N.I., Riosmena-Rodrıguez R., Paul-

Chavez L. (2010) Sponges associated with Sargassum spp.

(Phaeophyceae: Fucales) from the south-western Gulf of

California. Journal of the Marine Biological Association of the

United Kingdom, 90, 193–202.

Baldacconi R., Corriero G. (2009) Effects of the spread of the

alga Caulerpa racemosa var. cylindracea on the sponge

assemblage from coralligenous concretions of the Apulian

coast (Ionian Sea, Italy). Marine Ecology, 30, 337–345.

Blight A.J., Thompson R.C. (2008) Epibiont species richness

varies between holdfasts of a northern and a southerly

distributed kelp species. Journal of the Marine Biological

Association of the United Kingdom, 88, 469–475.

Bulleri F., Balata D., Bertocci I., Tamburello L., Benedetti-Cec-

chi L. (2010) The seaweed Caulerpa racemosa on Mediterra-

nean rocky reefs: from passenger to driver of ecological

change. Ecology, 91, 2205–2212.

Buschmann A.H., Gomez P. (1993) Interaction mechanisms

between Gracilaria chilensis (Rhodophyta) and epiphytes.

Hydrobiologia, 261, 345–351.

Carballo J.L., Naranjo S.A., Garcıa-Gomez J.C. (1996) The use

of sponges as stress indicators in marine ecosystems at

Algeciras Bay (southern Iberian Peninsula). Marine Ecology

Progress Series, 135, 109–122.

Conover J.T., Sieburth J.McN. (1964) Effect of Sargassum dis-

tribution on its epibiota and antibacterial activity. Botanica

Marina, 6, 147–157.

Contreras E.F. (2010) Ecosistemas Costeros Mexicanos. Una

actualizacion. Universidad Autonoma Metropolitana–Iztapa-

lapa, Mexico: 528 pp.

Cortes J. (2001) Requiem for an eastern Pacific seagrass bed.

Revista de Biologıa Tropical, 49, 273–278.

Crooks J.A. (2009) The role of exotic marine ecosystem engi-

neers. In: Rilov G., Crooks J.A. (Eds), Biological Invasions

in Marine Ecosystems: Ecological Management, and Geo-

graphic Perspectives, Ecological Studies 204. Springer, Berlin:

287–300.

Davis A.R., Roberts D.E., Cummins S.P. (1997) Rapid invasion

of a sponge-dominated deep-reef by Caulerpa scalpelliformis

(Chlorophyta) in Botany Bay, New South Wales. Australian

Journal of Ecology, 22, 146–150.

Dayton P.K. (1973) Dispersion, dispersal, and persistence of

the annual intertidal alga, Postelsia palmuetorformis Rupr-

echt. Ecology, 54, 433–438.

Doty M.S. (1961) Acanthophora, a possible invader of the mar-

ine flora of Hawaii. Pacific Science, 15, 547–552.

Eldredge L.G. (2003) Coral reef invasions. In: De Poorter M.

(ed.), Aliens. Invasive Species Specialist Group of the IUCN

Species Survival Commission, South Africa: 17, 9.

Fong P., Smith T.B., Wartian M.J. (2006) Epiphytic cyanobac-

teria maintain shifts to macroalgal dominance on coral reefs

following ENSO disturbance. Ecology, 87, 1162–1168.

Global Invasive Species Database (2010) Acanthophora spicifera.

Available from: http://www.issg.org/database/species/distribution.

asp?si=1060&fr=1&sts=&lang=EN (accessed 20 January 2011).

Glynn P.W., Mate J.L., Baker A.C., Calderon M.O. (2001)

Coral bleaching and mortality in Panama and Ecuador dur-

ing the 1997–98 El Nino–Southern Oscillation event: spa-

tial ⁄ temporal patterns and comparisons with the 1982–83

event. Bulletin of Marine Science, 69, 79–109.

Hauser A., Attrill M.J., Cotton P.A. (2006) Effects of habitat

complexity on the diversity and abundance of macrofauna

colonizing artificial kelp holdfasts. Marine Ecology Progress

Series, 325, 93–100.

Ingolfsson A. (1995) Floating clumps of seaweed around Ice-

land: natural microcosms and a means of dispersal for shore

fauna. Marine Biology, 122, 13–21.

Jephson N.A., Gray P.W.G. (1977) Aspects of the ecology of

Sargassum muticum (Yendo) Fensholt, in the Solent region

of the British Isles. The growth cycle and epiphytes. In:

Keegan B.F., Ceidigh P.O., Boaden P.J.S. (Eds), Biology of

Benthic Organisms. Pergamon Press, Oxford: 367–375.

Jimenez-Illescas A.R., Obeso-Nieblas M., Salas-De Leon D.A.

(1997) Oceanografıa fısica de la bahıa de La Paz, B.C.S. In:

Urban R.J., Ramırez M. (Eds), La bahıa de La Paz, Investiga-

cion y Conservacion. Universidad Autonoma de Baja Califor-

nia Sur, Centro Interdisciplinario de Ciencias Marinas,

Mexico and SCRIPPS Institute, La Paz: 31–41.

Kilar J.A., McLachlan J. (1986) Ecological studies of the alga

Acanthophora spicifera (Vahl) Borg. (Ceramiales: Rhodo-

phyta): vegetative fragmentation. Journal of Experimental

Marine Biology and Ecology, 104, 1–21.

Kottek M., Grieser J., Brck C., Rudolf B., Rubel F. (2006)

World map of the Koppen-Geiger climate classification

updated. Meteorologische Zeitschrift, 15, 259–263.

Leite F.P.P., Turra A. (2003) Temporal variation in Sargassum

biomass, Hypnea epiphytism and associated fauna. Brazilian

Archives of Biology and Technology, 46, 665–671.

Maldonado M., Uriz M.J. (1999) Sexual propagation by

sponge fragments. Nature, 398, 476.

Martınez-Nadal N.G., Rodriguez L.V., Casillas C. (1965) Isola-

tion and characterization of Sarganim complex, a new broad

spectrum antibiotic isolated from marine algae. Antimicro-

bial Agents and Chemotherapy, 1964, 131–134.

Mathieson A.C., Dawes C.J., Harris L.G., Hehre E.J. (2003)

Expansion of the Asiatic green alga Codium fragile subsp

tomentosoides in the Gulf of Maine. Rhodora, 105, 1–53.

Molina O.A. (2004) Estado Actual del Ecosistema Arrecifal de

Los Cobanos. FUNDARRECIFE ⁄ FIAES project 32.

Nonnis-Marzano C., Longo C., Corriero G. (2004) Modificazi-

oni distribuzionali in Halichondria panicea (Porifera, Demo-

spongiae) nel Lago di Lesina: un’alga non sessile come

vettore? Atti LXV Congresso Nazionale Unione Zoologica

Italiana, Giardini Naxos, Messina, 80, 21–25.

Obeso-Nieblas M., Shirasago-German B., Gavino-Rodrıguez J.,

Perez-Lezama E., Obeso-Huerta H., Jimenez-Illescas A.

(2008) Hydrographic variability in Bahıa de La Paz, Gulf of



California, Mexico (1995–2005). Revista de Biologıa Marina

y Oceanografıa, 43, 559–567.

O’Doherty D., Sherwood A.R. (2007) Genetic population

structure of the Hawaiian alien invasive seaweed, Acantho-

phora spicifera (Rhodophyta) as revealed by DNA sequenc-

ing and ISSR analyses. Pacific Science, 61, 223–233.

Pena V., Barbara I. (2006) Revision of the genus Dasya

(Ceramiales, Rhodophyta) in Galicia (NW Spain) and the

addition of a new alien species Dasya sessilis Yamada for the

European Atlantic coasts. Anales del Jardın Botanico de

Madrid, 63, 13–26.

Rodrıguez L.F. (2006) Can invasive species facilitate native

species? Evidence of how, when, and why these impacts

occur Biological Invasions, 8, 927–939.

Russell D.J. (1992) The ecological invasion of Hawaiian reefs

by two marine red algae, Acanthophora spicifera (Vahl)

Boerg. and Hypnea musciformis (Wulfen) J. Ag. and their

association with two native species, Laurencia nidifica J. Ag.

and Hypnea cervicornis J. Ag. ICES Marine Science Sympo-

sium, 194, 110–125.

Russell D.J., Balazs G.H. (1994) Colonization by the alien marine

alga Hypnea musciformis (Wulfen) J. Ag. (Rhodophyta: Gig-

artinales) in the Hawaiian Islands and its utilization by the

Green Turtle, Chelonia mydas L. Aquatic Botany, 47, 53–60.

Ryland J.S. (1974) Behaviour, settlement and metamorphosis of

bryozoans larvae: a review. Thalassia Jugoslavica, 10, 239–262.

Sanchez I., Fernandez C., Arrontes J. (2005) Long-term

changes in the structure of intertidal assemblages after inva-

sion by Sargassum muticum (Phaeophyta). Journal of Phycol-

ogy, 41, 942–949.

Schaffelke B., Hewitt C.L. (2007) Impacts of introduced

seaweeds. Botanica Marina, 50, 397–417.

Smith J.E., Hunter C.L., Smith C.M. (2002) Distribution and

reproductive characteristics of nonindigenous and invasive

marine algae in the Hawaiian Islands. Pacific Science, 56,

299–315.

Tsuda R.T., Coles S.L., Guinther E.B., Finlay O., Andrew R.,

Harris F.L. (2008) Acanthophora spicifera (Rhodophyta:

Rhodomelaceae) in the Marshall Islands. Micronesica, 40,

245–252.

Underwood A.J. (1997) Experiments in Ecology: Their Logical

Design and Interpretation Using Analysis of Variance. Cam-

bridge University Press, Cambridge: 504 pp.

Wallentinus I., Nyberg C.D. (2007) Introduced marine organ-

isms as habitat modifiers. Marine Pollution Bulletin, 55,

323–332.

Withers R.G., Farnham W.F., Lewey S., Jephson N.A., Hay-

thorn J.M., Gray P.W.G. (1975) The epibionts of Sargassum

muticum in British waters. Marine Biology, 31, 79–86.

Witman J.D., Suchanek T.H. (1984) Mussels in flow: drag and

dislodgement by epizoans. Marine Ecology Progress Series, 16,

259–268.



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