Hydrobiologia (2006) 555:263–269 Springer 2006 H. Queiroga, M.R. Cunha, A. Cunha, M.H. Moreira, V. Quintino, A.M. Rodrigues, J. Seroˆdio & R.M. Warwick (eds), Marine Biodiversity: Patterns and Processes, Assessment, Threats, Management and Conservation DOI 10.1007/s10750-005-1122-4
The colonisation of human-made structures by the invasive alga Codium fragile ssp. tomentosoides in the north Adriatic Sea (NE Mediterranean) Fabio Bulleri1,2,*, Marco Abbiati1,2 & Laura Airoldi1,2 1 Centro Interdipartimentale di Ricerca per le Scienze Ambientali di Ravenna Universita` di Bologna, Via S.Alberto 163, I-48100, Ravenna, Italy 2 Dipartimento di Biologia Evoluzionistica Sperimentale (*Author for correspondence: E-mail:
[email protected])
Key words: invasive species, human-made structures, Codium fragile, Adriatic Sea, wave-exposure
Abstract Human-made structures, such as groynes, breakwaters, seawalls, pier pilings and floating pontoons, are becoming common features of the landscape in urbanised coastal and estuarine areas. Despite this tendency few studies have focused on their ecology or on their potential impacts on natural assemblages of organisms. When artificial structures are introduced in areas with little or no hard substrata, they not only provide novel habitats, which enables the colonisation of sandy areas by hard-bottom dwelling species, but they can also provide suitable habitats for exotic species. Along the north-east coast of Italy, sandy shores are protected from erosion by a line of breakwaters, which runs almost uninterrupted for about 300 km. These structures provide habitat for a variety of macroalgae and invertebrates and also for the invasive green alga Codium fragile ssp. tomentosoides. The aim of this study was, therefore, to investigate patterns of distribution of this alga on breakwaters in Cesenatico. In particular, we compared the density of thalli, biomass, length and degree of branching of C. fragile ssp. tomentosoides between the landward and the seaward sides of breakwaters, to test the hypothesis that sheltered habitats (landward) represent more suitable habitats than exposed habitats (seaward). In general, the landward side of breakwaters supported greater numbers of thalli of C. fragile ssp. tomentosoides than seaward sides. Thalli grew longer and more branched in sheltered habitats, leading to an overall larger biomass of the alga on the landward side of breakwaters. The presence of sheltered human-made hard substrata in the vicinity of major trading ports and sources of eutrophication could enhance the dispersal of invasive species across regional and geographic scales. Thus, the effects of artificial structures and introduced species on coastal assemblages cannot be evaluated separately, but their synergistic nature should be considered in planning strategies for conservation of biodiversity in coastal habitats.
Introduction The human population on Earth is rapidly expanding and about 70% of people live on or within 60 km from the coast (Hammond, 1992). This percentage is increasing (Hammond, 1992; Gray, 1997) and it is predicted that the population living on the coast will double in the next 30 years (Reilly et al., 1996; Gray, 1997). As a consequence, human-made structures, such as pier pilings, breakwaters, jetties, seawalls
and floating pontoons, are becoming common features of the landscape in coastal and estuarine regions of developed countries (Glasby & Connell, 1999). Despite this tendency, few studies have focused on changes in the distribution and abundance of organisms caused by the introduction of human-made structures in shallow coastal waters, either on hard (Connell & Glasby, 1998; Glasby & Connell, 1999; Chapman & Bulleri, 2003) or soft bottoms (Davis et al., 1982; Page et al., 1999).
264 In the case in which human-made structures are introduced in areas with little or no hard substrata, their effects are not limited to the provision of novel habitats, but they can also alter natural patterns of distribution of marine organisms (Glasby & Connell, 1999). Human-made substrata may, in fact, function as stepping stones, enabling larvae and propagules of many marine invertebrates and algae that disperse over short distances (e.g., Jackson, 1986; Santelices, 1990) to colonise areas outside their natural ranges of distribution. A primary concern is that exotic species could take advantage of introduced human-made substrata, thus affecting species composition and biodiversity at local and regional scales (Glasby & Connell, 1999). Along the north-east coast of Italy (Adriatic Sea), natural rocky reefs are rare and over 60% of the coastline is characterised by the presence of hard structures for protection against erosion of shores. Among these structures, breakwaters, which run parallel to the coast, provide shelter (i.e., landward side) and exposed (i.e., seaward side) hard-bottom habitats suitable for colonisation of a diverse assemblage of macroalgae and invertebrates (Bacchiocchi & Airoldi, 2003), including the invasive green alga Codium fragile (Sur.) Hariot ssp. tomentosoides (van Goor) Silva. This species, which has become a locally major component of assemblages on temperate rocky shores throughout the world (Trowbridge, 1998), was first sighted in the Mediterranean Sea in 1950, and attained its peak of abundance in the early 1960s, stabilising at lower levels afterwards (Boudouresque, 1994). The most likely vectors of introduction of C. fragile ssp. tomentosoides in the Mediterranean Sea have been identified as ship hulls and activities involving translocation of oysters (Ribera, 1994). Furthermore, the presence of sheltered habitats in close proximity to vector vessels and sources of nutrient enrichment, such as those provided along the north-east coast of Italy by harbours, coastal lagoons and breakwaters (e.g., Correggiari et al., 1992) has been suggested to increase the establishment and/or persistence of C. fragile ssp. tomentosoides (Trowbridge, 1998, 1999). The aim of this study was to quantify patterns of distribution and abundance of C. fragile ssp. tomentosoides in low-shore habitats of breakwaters in the north Adriatic Sea and to evaluate whether
the provision of sheltered habitats by breakwaters could enhance the colonisation and persistence of this invasive alga. Specifically, we tested the hypotheses that the abundance, biomass, length and degree of branching of thalli of C. fragile ssp. tomentosoides would be greater on the landward (sheltered) than on the seaward (exposed) side of breakwaters and that these patterns would be consistent among breakwaters 100s of metres apart and between times of sampling.
Materials and methods Study site This study was done in low-shore habitats (0– 20 cm above the mean level of low water; MLLW) on the breakwaters at Cesenatico (Emilia Romagna, Italy, Fig. 1) in summer 2003. This area is subject to moderate wave-action and is characterised by a relatively large tidal amplitude (about 80 cm), in comparison to other regions of the Mediterranean Sea. Natural rocky reefs are absent in this area, the closest occurring at Gabicce (about 50 km south) and Trieste (about 300 km north). The region is characterised by the almost uninterrupted presence of groynes and offshore breakwaters, which were built to prevent erosion of sandy shores. At Cesenatico, breakwaters are made of large calcareous boulders, about 0.5–2 m in diameter. They were about 100 m long, 200 m offshore and spaced about 50 m apart. A general description of the study area and assemblages on coastal defence structures can be found in Bacchiocchi & Airoldi (2003) and references therein. The invasive subspecies Codium fragile ssp. tomentosoides can be distinguished from the native Mediterranean species Codium vermilara (Olivi) Delle Chiaje by the shape of utricules (Silva, 1955). The observation of several 10 s of specimens under a microscope indicated the presence of monospecific stands of C. fragile ssp. tomentosoides in low-shore habitats of the breakwaters. During the present study (June–July 2003) reproductive structures (gametangia) were not found, while subsequent observations indicated that in the study area C. fragile ssp. tomentosoides was fertile in mid-August until the end of September. In the study area, C. fragile ssp. tomentosoides is present
265 randomly chosen boulders. The size of the plots was chosen according to the results of previous pilot studies (Airoldi et al., 2000), which indicated that plots of 20 · 20 cm were the most efficient to sample the small and irregular surfaces of the blocks used to build the breakwaters. Ten thalli of C. fragile ssp. tomentosoides were also collected at random from each boulder and the biomass (wet weight), length and degree of branching (maximum number of branch dichotomies from stipe to branch tips) of each frond arising from each holdfasts were measured in the laboratory within a few hours. When more than one frond was generated by a single holdfast the average length was used in the analysis. Incipient fronds (1–5 mm) were not taken into account. Sampling was repeated in June and July 2003. Different boulders were sampled on each date, in order to obtain data independent through time. Data were analysed by 4-way ANOVAs, including the factors Time (random), Exposure (fixed and orthogonal), Breakwater (random and orthogonal) and Boulder (random and nested within the interaction Time Exposure · Breakwater). When appropriate, pooling procedures were used following Winer et al. (1991). Cochran’s test was used to test for heterogeneity of variances (Winer et al., 1991) and data were transformed when necessary. SNK tests were used for a posteriori comparison of the means (Winer et al., 1991). Figure 1. Map showing the study area (Cesenatico) and the closest natural rocky reefs up north (Trieste) and down south (Gabicce, Rimini).
as visible macroscopic fronds for a few months during the spring and summer (Airoldi, pers. obs.), while basal holdfasts are likely to be perennial, as reported by other authors (reviewed in Trowbridge, 1996, 1999). Sampling design and analysis Three breakwaters were randomly selected 100s of metres apart in spring 2003 and were sampled on the seaward and on the landward side. On each breakwater, the density (number of thalli per surface unit) of C. fragile ssp. tomentosoides was sampled in five 20 · 20 cm plots on each of three
Results The density of thalli of C. fragile ssp. tomentosoides was generally greater on the landward than on the seaward side of breakwaters, but differences between exposures were significant only in July, when number of thalli greatly decreased on the seaward sides (Fig. 2a; Table 1). The density of thalli did not vary among similarly exposed sides on different breakwaters, whilst it differed among boulders within sides (Table 1). The weight and length of thalli of C. fragile ssp. tomentosoides were greater on the landward than on the seaward side of breakwaters (Fig. 2b and c; Table 1). Differences between exposures increased from June to July, due to the growth in size of the alga on the landward sides (Fig. 2; Table 1). The weight varied among breakwaters in July, but not
266 Discussion
Figure 2. Mean (+SE) of density (a; n = 5), weight (b; n = 10), length (c; n = 10) and degree of branching (d; n = 10) of thalli of Codium fragile ssp. tomentosoides on the landward and the seaward side of breakwaters, in June and July 2003.
in June, resulting in a significant Time · Breakwater interaction (Table 1). The length of thalli varied among boulders (Table 1). The order of branching of thalli of C. fragile ssp. tomentosoides was significantly greater on the landward than on the seaward side of breakwaters (Fig. 2d; Table 1). There was large variability among breakwaters in the degree of thallus branching, which changed from June to July.
The invasive green alga C. fragile ssp. tomentosoides has become a major component of coastal assemblages along the north-east sandy coast of the Adriatic Sea. The results of this study indicate that artificial structures have greatly contributed to the expansion of this species, by providing hard substrata suitable for its colonisation. In July, the landward side of breakwaters supported greater numbers of thalli of C. fragile ssp. tomentosoides than the seaward side. Thalli grew longer and more branched in sheltered habitats, leading to an overall larger biomass of the alga on the landward side of breakwaters. These differences were consistent across breakwaters, indicating that relevant ecological processes that produced them (e.g., recruitment and post-recruitment mortality) operated consistently at the scale of 100s of metres. Differences between the landward and seaward sides also increased from June to July, which is the period of time encompassing the peak of growth of C. fragile ssp. tomentosoides (F. Bulleri, pers. obs.) This temporal trend was related to both greater rates of growth of the alga on the landward sides of breakwaters and higher rates of mortality of thalli on the seaward sides, probably due to dislodgement by wave-action. Recruitment of C. fragile ssp. tomentosoides was not limited in wave-swept habitats of the breakwaters and specialised grazers (sacoglossan slugs) were not observed on the structures. It has been, however, reported that larger thalli of C. fragile ssp. tomentosoides can be removed by waves more easily (Trowbridge, 1998, 1999). It is likely that thalli that had grown to a critical size (length) could not persist in the stressful hydrodynamic conditions on the seaward sides of breakwaters during summer swells. Overall, these results are in accordance with those of other studies (Trowbridge, 1995, 1996), which have described C. fragile ssp. tomentosoides as a species best performing in protected or moderately exposed habitats. Besides the occurrence of suitable sheltered habitats on the breakwaters, other factors could have promoted the establishment and persistence of C. fragile ssp. tomentosoides in the study area. The successful establishment of exotic species in
267 Table 1. Analyses and SNK tests on the effects of Time, Exposure, Breakwater and Boulder on (A) density, (B) biomass, (C) length and (D) degree of branching of thalli of C. fragile ssp. tomentosoides. When appropriate, pooling procedures were used following Winer et al. (1991); because Time and Breakwater are random factors, some tests were only possible after elimination of terms (not significant at P = 0.25; Winer et al. 1991; Underwood 1997). §Degrees of freedom of the Residual for Biomass, Length and Branching * P < 0.05; ** P < 0.01; *** P < 0.001. Source of variation
A) Density df
MS
B) Biomass F
MS
C) Length F
D) Branching
MS
F
MS
F
Time = T
1
1.80
2.56
10.33
0.74
729.36
39.03*
2.12
4.68
Exposure = E Breakwater= B
1 2
1.06 0.01
no test 0.01
333.93 2.02
38.64 0.15
775.16 1.12
no test 0.06
6.82c 0.10
125.19** 0.23
T·E
1
6.59
21.22*
eliminated
T·B
2
0.70
0.66
13.87
E·B
2
0.69
2.21
T·E·B Boulder(T · E · B) Residual
8.64a
8.56*
86.61b
7.86**
0.11
11.14***
18.69
1.70
0.45
6.68**
0.13
pooled
15.93
1.45
0.05
0.44
2
0.31
0.29
1.89
pooled
9.71
24
1.07
2.30**
1.24
1.48
11.01
144 324§ 0.47
0.84
eliminated 0.12 2.05**
5.37
0.07 0.05
Transformation
Ln (x + 1)
Ln (x + 1)
None
Ln (x + 1)
Cochran’s test
NS
NS
P < 0.01
NS
SNK tests
A) Density
B) Biomass
C) Length
SE = 0.08 June: Landward =
SE = 0.11 June: Landward >
SE = 0.35 June: Landward >
Seaward
Seaward
Seaward
July: Landward > July: Landward >
July: Landward >
Seaward
Seaward
Seaward
1.82 1.31
a Tested against the pooled term B · E + T · E · B(MS=1.01, df = 4); b Tested against the term Boulder (T · E · B); c Tested against the term E · B.
new areas has been shown to be related to their life-history attributes (Trowbridge, 1995, 1998). C. fragile ssp. tomentosoides exhibits rapid growth, and regeneration from filaments (vaucherioid stage), while fragments confer high dispersal ability on this alga. Furthermore, parthenogenetic gametes enable the persistence of populations even at low densities. C. fragile ssp. tomentosoides exhibits tolerances to salinities ranging from 12.5 to 40 ppt (reviewed in Trowbridge, 1998), inhabiting both estuarine and marine habitats. There is also evidence that C. fragile ssp. tomentosoides can be enhanced by eutrophication of waters, this alga being able to exploit different sources of nitrogen, including nitrate, nitrite, ammonia and urea (Hanisak, 1979). The ability of Codium fragile ssp. tomentosoides to establish in new regions could also depend upon attributes of native assemblages of organisms and interactions with local environmental conditions (reviewed by Trowbridge, 1998, 1999). The
establishment of an invader species, such as C. fragile ssp. tomentosoides, may be favoured by vacant niches and low diversity of species (Ribera & Boudoresque, 1995; Trowbridge, 1995; Tilman, 1997; Levin et al., 2002). Indeed, along the northeast coast of Italy, Bacchiocchi & Airoldi (2003) have shown that the diversity of species on humanmade structures is generally low and they have reported a relatively large amount of unoccupied space. The causes underlying this low diversity and abundance of species are not well understood. The study area, being under the influence of the Po river plume, is subject to abrupt changes in salinity and turbidity and to high nutrient loads (Correggiari et al., 1992; Zavatarelli et al., 1998). These relatively harsh physical conditions could prevent or slow down colonisation of space on breakwaters by many taxa of macroalgae and invertebrates, thus lessening the intensity of intra-specific competition and enabling the tolerant C. fragile ssp. tomentosoides to settle and persist at low-shore levels.
268 Furthermore, breakwaters are subject to frequent disturbances, either natural (e.g., storms) or anthropogenic (e.g., maintenance works, harvesting of invertebrates for food). These disturbances could indirectly enhance the recruitment of C. fragile ssp. tomentosoides by removing the mussel Mytilus galloprovincialis Lamarck, which is the main spaceoccupier at low-intertidal and shallow subtidal levels on breakwaters. Although assemblages on artificial structures cannot be referred to as ‘natural’, experimental work is needed to identify the interactions between ‘native’ and exotic species on breakwaters and the environmental factors that modulate them. Overall, these results suggest that by providing hard and sheltered substrata within sandy exposed habitats, artificial structures have the potential to alter biodiversity not only by attracting benthic species from nearby natural reefs and coastal lagoons (Bacchiocchi & Airoldi, 2003), but also by enabling the incursion of exotic species. There are numerous examples of introduced species, including algae and invertebrates, that have established in enclosed waters characterised by intense shipping activities and sources of eutrophication (OcchipintiAmbrogi & Savini, 2003 and references therein). Indeed, the impact of human-made structures on natural assemblages would be largely underestimated without evaluating the risks of introducing exotic species. Similarly, no reliable predictions of local to regional pathways of spreading of invasive species can be formulated without embodying the influence of anthropogenic alterations to coastal landscapes. Even though human-made structures would represent sub-optimal habitats for exotic species, for their increasing presence, they could act as stepping stones (Glasby & Connell, 1999), promoting the expansion of invaders to areas that would be naturally isolated. Thus, the effects of human-made structures and introduced species on assemblages of organisms cannot be evaluated separately, but their synergistic nature should be considered in order to plan sound strategies for the conservation of biodiversity in coastal habitats.
Acknowledgements We sincerely thank M. Carrera, S. Santin and G. Branca for help in the field and in the lab and C. Trowbridge and one anonymous referee for
valuable comments on an earlier draft. This work was supported by funds from the EU project DELOS (EVK3-CT-2000–00041) and from the project COFIN (ex 40%) to M.A. L.A. was supported by an ‘Assegno di Ricerca’ from the Universita` di Bologna.
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