Mar Biol (2016) 163:161 DOI 10.1007/s00227-016-2937-4
INVASIVE SPECIES - REVIEW PAPER
The invasion of Caulerpa cylindracea in the Mediterranean: the known, the unknown and the knowable L. Piazzi1 · D. Balata2 · F. Bulleri3 · P. Gennaro4 · G. Ceccherelli1
Received: 1 December 2015 / Accepted: 13 June 2016 © Springer-Verlag Berlin Heidelberg 2016
Abstract The spread of the green macroalga Caulerpa cylindracea is one of the most threatening invasions in the Mediterranean Sea. Many correlative and experimental studies have focused on different aspects of C. cylindracea invasion. This paper aims to evaluate the main factors influencing the spread of this alga through an overview of the results from 47 published papers on this topic; a conceptual model synthesizing the main biotic and abiotic factors that influence C. cylindracea spread was proposed. Mechanical destruction of habitats, enhanced sedimentation rate and nutrients loading directly promote the spread of C. cylindracea. Indirect effects due to factors that foster the spread of turf-forming algae at the expense of canopy-forming species and decrease substrate complexity emerged as an important determinant of the success of C. cylindracea. Ultimately, the spread of C. cylindracea appears to be regulated by a complex net of interactions between abiotic and biotic factors. Our conceptual model represents a general tool for the rapid assessment
Responsible Editor: K. Bischof. Reviewed by Ch. Hewitt and an undisclosed expert. This article is part of the Topical Collection on Invasive Species. * L. Piazzi
[email protected] 1
Dipartimento di Scienze della Natura e del Territorio, Università di Sassari, Via Piandanna 4, 07100 Sassari, Italy
2
Tenuta San Beda, via Carmignani 18, 55015 Montecarlo (Lu), Italy
3
Dipartimento di Biologia, Università di Pisa, Via Derna 1, 56126 Pisa, Italy
4
Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA ex ICRAM), Rome, Italy
of the factor underpinning the spread of non-native species, a critical step for the control of non-native species that have successfully established viable populations.
Introduction Biological invasions are among the most severe threats to biodiversity worldwide (Vitousek et al. 1996, 1997; Mack et al. 2000). Since devastating effects of exotics on the biodiversity and functioning of recipient ecosystems have been widely documented (Pimentel et al. 2001), understanding the mechanisms regulating species invasions has become a pressing need both to predict pathways of invasion and to control the spread (Anderson 2007; Gollasch 2007; Hewitt and Campbell 2007). In fact, the knowledge of mechanisms facilitating the establishment and enhancing the competitiveness of an invader can allow managing the invasion by addressing efforts toward the mediating factors rather than the invader itself (Didham et al. 2005). However, the mechanisms involved in invasions are often not evident. In fact, environmental factors may directly influence the spread of invasive species, by increasing growth rate or reproductive efficiency (Didham et al. 2005), but they can also act indirectly, by decreasing habitat resistance to invasion (Piola and Johnston 2008). Moreover, complex interactions among biotic and abiotic factors can often occur and synergistic effects may be difficult to detect (Dukes and Mooney 1999; Harris and Tyrrell 2001; Stachowicz et al. 2002). Within this context, the development of conceptual models may be a useful tool to synthesize complex interactions among factors and mechanisms involved in biological invasions (Airoldi et al. 2008). The spread of the green macroalga Caulerpa cylindracea Sonder (Belton et al. 2014) is one of the most
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threatening invasions in the Mediterranean Sea (Piazzi et al. 2005b; Montefalcone et al. 2015b). C. cylindracea has rapidly and successfully invaded wide areas of this Basin (Piazzi et al. 2005b; Klein and Verlaque 2008), modifying the structure of invaded assemblages (Piazzi et al. 2001b; Vázquez-Luis et al. 2008; Klein and Verlaque 2009) by reducing alpha and beta diversity (Piazzi and Balata 2008 2009; Žuljević et al. 2011). Many correlative and experimental studies have examined different aspects of C. cylindracea invasion and identified several factors enhancing the spread (Piazzi et al. 2003b; Ceccherelli et al. 2002, 2014; Bulleri and Benedetti-Cecchi 2008; Bulleri et al. 2011; Gennaro and Piazzi 2014) and competitive ability of the alga with respect to native species (Piazzi et al. 2005a, 2007b; Bulleri and Piazzi 2015; Gennaro et al. 2015), but also highlighting complex interactions among factors (Gennaro and Piazzi 2014; Tamburello et al. 2014; Balata et al. 2015). Here, we assessed the main factors influencing the spread of C. cylindracea by synthesizing current knowledge generated by both correlative and experimental studies. A conceptual model was developed in order to facilitate the identification of the main interactions and feedbacks among the factors that influence the spread of C. cylindracea. The main purpose of this model is that of fostering the identification of potential gaps in knowledge and, hence, of identifying priority areas of further research.
Materials and methods Relevant literature on the Mediterranean C. cylindracea (ex Caulerpa racemosa and C racemosa var. cylindracea) was searched using the ‘Science Citation Index Expanded Database’ on a Web research platform (ISI Web of Science). Proceedings of the main Mediterranean workshops on marine biology from 1992 (International Workshops on Caulerpa taxifolia, GIS Posidonie publ., Mediterranean Symposiums on marine vegetation, UNEP-RAC/SPA publ., Congress of Italian Society of Marine Biology, SIBM publ.) were also examined. Among all the papers retrieved, those reporting factors influencing the spread of the alga were selected. In this contest, the factors influencing C. cylindracea spread are meant those that facilitate or inhibit the establishment, the dispersal, the growth and the competitiveness of the alga.
Results (the known) A total of 206 papers concerning distribution, ecology, biology and biochemistry of the Mediterranean specimens of C. cylindracea were retrieved from the literature. Among
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them, 47 papers reporting information about C. cylindracea spread were selected (Table 1). Correlative and experimental studies suggest that C. cylindracea spread (dispersal, establishment, growth and competitiveness) may be influenced by abiotic factors (substrate complexity and water movement) and biotic interactions with native primary producers (e.g., canopy-forming macrophytes and turf-forming), and herbivores and with other invaders. Moreover, anthropogenic pressures (eutrophication, increased sedimentation, physical habitat destruction and overfishing) can influence the spread of the alga acting directly on C. cylindracea growth rates or reproductive ability, but also indirectly by altering the strength of natural forces able to control spread of the seaweed (Fig. 1). Human alterations of biotic and abiotic factors can influence the growth of the alga, the anchorage of rhizoids, the exploitation of resources and the dispersal of fragments (Table 2). Substrate complexity In marine rocky habitats, topographic heterogeneity and complexity of substrates (Beck 2000) are important determinants of species distribution and abundance (Archambault and Bourget 1996; Lapointe and Bourget 1999), influencing biotic interactions and settlement and/or recruitment of sessile organisms (Gosselin and Bourget 1989; Bourget et al. 1994; Bourget and Harvey 1998). Likewise, they have been found to regulate the spread dynamics of biological invasions (Tamburello et al. 2013). For C. cylindracea, several data support the facilitative model of topographic heterogeneity for the invasive spread (Fig. 1), as rhizoids need suitable substrates for the anchoring. Substratum complexity has been shown to augment the spread of the C. cylindracea in rocky habitats probably favouring the ‘rooting’ of rhizoids and, consequently, the growth of stolons (Fig. 2; Bulleri et al. 2009; Balata et al. 2015). In particular, greater penetration of C. cylindracea stolons has been documented in experimental areas dominated by encrusting Corallinales than on bare rock surfaces, suggesting that living corallines, being characterized by pits and ridges, may facilitate the hold of stolons on the substratum (Bulleri et al. 2009). This mechanism would also explain the evidence that in the Mediterranean Sea dead mat of the seagrass Posidonia oceanica (high topographic complexity habitat) is the most favorable substratum for the colonization of C. cylindracea (Piazzi et al. 2001b; Ruitton et al. 2005b; Infantes et al. 2011; Piazzi and Balata 2009). In soft bottoms, the texture of substratum would be crucial to the spread of C. cylindracea. In general, detritic bottoms with coarse texture facilitate the spread of the alga more than fine sand (Pacciardi et al. 2011). This pattern becomes particularly relevant in rhodolite beds, biogenic
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Table 1 List of papers considered in the review References
Complexity of bottom
Balata et al. (2015) Bernardeau-Estellier et al. (2015)
+
Water movement
Canopy Algal Herbivores Other Eutrophicamacrophytes turfs invaders tion
+
Bulleri and Malquori (2015) Bulleri and Piazzi (2015) Bulleri et al. (2009) Bulleri et al. (2010) Bulleri et al. (2011) Caronni et al. (2015) Cebrian et al. (2011) Ceccherelli and Piazzi (2001)
+ +
Ceccherelli et al. (2000) Ceccherelli et al. (2002) Ceccherelli et al. (2014) Gennaro and Piazzi (2011) Gennaro and Piazzi (2014) Gennaro et al. (2015) Incera et al. (2010) Infantes et al. (2011) + Ivesa et al. (2015) Katsanevakis et al. (2010) Klein and Verlaque (2008) Klein and Verlaque (2009) + Klein and Verlaque (2011) Marin-Guirao et al. (2015) Montefalcone et al. (2010) Montefalcone et al. (2015a) Pacciardi et al. (2011) + Piazzi and Balata (2009) Piazzi and Ceccherelli (2002)
+
+ − − −
+
−
− −
+
− −
+
+
+
+
+
+ + +
−
− − −
− − − −
Piazzi and Ceccherelli (2006) Piazzi et al. (2001a) Piazzi et al. (2001b) Piazzi et al. (2003a) Piazzi et al. (2003b) Piazzi et al. (2005a) Piazzi et al. (2007b) Piazzi et al. (2014) Ruitton et al. (2005b) Ruitton et al. (2006) Tamburello et al. (2013) Tamburello et al. (2014) Tomas et al. (2011a)
Mechanical destruction
+
−
Bulleri and BenedettiCecchi (2008)
Sedimentation
+
+
0
+ 0 +
0 +
+
−
−
+
+ + +
0 + −
−
+
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Table 1 continued References Tomas et al. (2011b) Vaselli et al. (2008) Žuljević et al. (2008)
Complexity of bottom
Water movement
Canopy Algal Herbivores Other Eutrophicamacrophytes turfs invaders tion
−
Sedimentation
Mechanical destruction
− −
+ = enhancing effect, − = inhibiting effect, = 0 neutral effect
structures built by free-living Corallinales on sandy bottoms (Foster 2001). These bottoms are particularly suitable to the spread of C. cylindracea as they provide a complex three-dimensional substrate for stolon attachment (Klein and Verlaque 2009; Piazzi personal observation). Canopy‑forming and turf‑forming macrophytes Vulnerability to invasions changes among habitats (Wasson et al. 2005), as the ecological properties of the recipient assemblages can be crucial to determine the resistance to invaders (Valentine et al. 2007). Resistance to invasions may be related to biodiversity, as highly diversified communities may be less susceptible to invasions (Stachowicz et al. 2002), but also to the functional composition of assemblages (Arenas et al. 2006; Britton-Simmons 2006; Dunstan and Johnson 2007). Several correlative and experimental studies highlighted that morphological traits of recipient assemblages can be more important than diversity in determining resistance of macroalgal assemblages to C. cylindracea invasion (Ceccherelli et al. 2002; Piazzi and Balata 2009; Bulleri et al. 2010; Gennaro and Piazzi 2014). In particular, C. cylindracea seems to spread preferentially in urbanized coasts (Ruitton et al. 2005b; Bulleri et al. 2011; Ivesa et al. 2015). The human-induced degradation of habitats seems to facilitate the spread of the alga (Montefalcone et al. 2010; Bulleri et al. 2011), as the shift from canopy habitat to algal turfs seems to be the main factor enhancing C. cylindracea invasion (Fig. 1; Bulleri et al. 2010, 2011). In fact, the occurrence of dense canopy assemblages both formed by seaweeds or seagrasses inhibits the invasion (Fig. 3; Bulleri et al. 2010; Katsanevakis et al. 2010; Ceccherelli et al. 2014), while C. cylindracea spread is facilitated by the presence of algal turfs (Fig. 4; Ceccherelli et al. 2002; Piazzi et al. 2003b; Bulleri and Benedetti-Cecchi 2008; Gennaro and Piazzi 2014). In the Mediterranean Sea, canopy habitats are constituted by meadows of the seagrass P. oceanica (L.) Delile and by macroalgae belonging to the order Fucales (Cystoseira spp. and Sargassum spp.). Several studies have shown that the clearing or thinning of stands of canopy-forming species, both algae and seagrasses, is generally more
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heavily colonized by C. cylindracea (Katsanevakis et al. 2010; Bulleri et al. 2010, 2011; Ceccherelli et al. 2014). Experimental studies have also shown that no C. cylindracea was found inside seagrass meadow independently of disturbance, while, at the edge, the cover of C. cylindracea was enhanced when rhizomes had been damaged (Ceccherelli et al. 2014). Also the growth of C. cylindracea at the edge of meadows is regulated by seagrass architecture: stolon elongation and percent cover of C. cylindracea were significantly higher where seagrass shoot density was reduced to 10 % of the natural density (Ceccherelli et al. 2000). The mechanisms involved are difficult to identify as the presence of the canopy can influence invasion success both directly and indirectly. Shading is one of the main alterations that canopies can produce. C. cylindracea appears to have a high photoacclimative plasticity, allowing the colonization of deep subtidal habitats (Capiomont et al. 2005; Piazzi et al. 2007a), although photoacclimation is hypothesized to have an energy cost (Bernardeau-Esteller et al. 2015). Results obtained from mesocosm and field experiments have consistently shown that light levels inside seagrass canopy strongly limit its photosynthetic performance and lead to a carbon balance unable to sustain algal development (Bernardeau-Esteller et al. 2015; Marin-Guirao et al. 2015). Although light availability seems to play a major role in the resistance of seagrass meadows to the invasion by C. cylindracea, other factors related to the canopy may occur. For example, the sweeping of the substratum by algal fronds or seagrass leaves could mechanically prevent the reattachment of fragments of the seaweed such as documented in kelp habitat (Irving and Connell 2006). In canopy assemblages, C. cylindracea is thought to act simply as a passenger (sensu MacDougall and Turkington 2005) of habitat degradation (Bulleri et al. 2010). However, where no Fucales or P. oceanica are present, the invader can cause strong regression of erect macroalgae (Piazzi et al. 2001b, 2007a; Piazzi and Balata 2008, 2009; Klein and Verlaque 2011). Moreover, C. cylindracea could be the driver for P. oceanica loss in shallow meadows, as observed in the Ligurian Sea, where healthy meadows have declined after the establishment of the alga (Montefalcone
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ANTHROPIC PRESSURES
enhance
physical destruction
inhibit fishing
increased sedimentation
161
uncertain effects
eutrophication
herbivory
substrate complexity
canopy macrophytes
C. cylindracea spread
ABIOTIC FACTORS water movement
algal turfs
BIOTIC FACTORS
other invaders
Fig. 1 Conceptual model showing factors influencing Caulerpa cylindracea spread
et al. 2010). Once C. cylindracea has established, often following a regression of macroalgal canopies, it can subsequently prevent the recovery of native populations by facilitating the persistence of alternative assemblages dominated by stress-tolerant species (Bulleri et al. 2010; Montefalcone et al. 2015a). Recent studies have, however, shown that the effects of canopy formers on the spread of C. cylindracea can be highly variable even among species belonging to the same genus. Indeed, the spread of C. cylindracea was found to be fostered by Cystoseira crinita, little influenced by Cystoseira barbata and reduced by Cystoseira compressa (Bulleri et al. 2016). Thus, even relatively subtle differences in life traits (e.g., size, degree of branching, tissue texture) of canopy formers might be sufficient to generate opposite effects on the establishment and spread of C. cylindracea. This suggests that clumping canopy-forming species into a single group is not warranted and, more generally, that phylogenetic similarity does not necessarily imply functional similarity (Bulleri et al. 2016).
Algal turfs can enhance C. cylindracea spread both favouring the establishment of fragments (Ceccherelli and Piazzi 2001) and providing a suitable substrate for the anchoring of the rhizoids (Ceccherelli et al. 2002; Piazzi et al. 2003b; Bulleri and Benedetti-Cecchi 2008). In fact, the three-dimensional matrix of turfs may be very effective in collecting and trapping debris drifting on the bottom, including sediments and fragments of C. cylindracea (Ceccherelli and Piazzi 2001). Algal turfs can also provide a suitable substrate for prostrate stolons of C. cylindracea to anchor, in comparison with lower-complexity habitats such as encrusting coralline-dominated surfaces (Ceccherelli et al. 2002; Piazzi et al. 2003b; Bulleri and BenedettiCecchi 2008). This result was consistent regardless of the type of substratum (either natural or artificial), suggesting the physical positive effects of turfs on the C. cylindracea spread (Bulleri and Benedetti-Cecchi 2008). However, turf may also indirectly facilitate C. cylindracea spread, since it can act as sediment trap (Airoldi 2003), an even more suitable condition for the spread of rhizotrophic species such as
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Table 2 Mechanisms of influence of the main factors enhancing or inhibiting the spread of Caulerpa cylindracea Enhancing mechanisms
Inhibiting mechanisms
Complexity of bottom Water movement Canopy macrophytes Algal turfs Herbivores Other invaders Eutrophication Sedimentation Mechanical destruction
Anchorage of rhizoids, trapping of sediment Fragment dispersal – Anchorage of rhizoids, trapping of sediment Fragmentation, growth stimulation Anchorage of rhizoids, trapping of sediment Enhanced growth, shift from canopy to turfs Availability of nutrients, shift from canopy to turfs Destruction of canopy
– Direct disturbance Low light, abrasion – Removal Direct and indirect competition – Abrasion Direct disturbance
Fishing
Canopy removal, fragment dispersal
–
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Percent cover
Fig. 2 Mean (+SE) percent cover of Caulerpa cylindracea (a) at different complexities (from Balata et al. 2015) and (b) at different substrate, bare rock or encrusting corallines (from Bulleri et al. 2009)
6
(A)
10
5
8
4
6
3
4
2
2
1
0
0 low complexity
Caulerpales (Chisholm et al. 1996; Ceccherelli and Cinelli 1997). A reciprocal facilitation has been observed between C. cylindracea and turfs (Bulleri et al. 2010): C. cylindracea deeply affects encrusting, epilithic and some erect species (Piazzi et al. 2001b; Balata et al. 2004), while opportunistic filamentous turf-forming species can co-occur with the alga (Piazzi et al. 2001b; Piazzi and Balata 2008; Gennaro and Piazzi 2011). Therefore, although phenology of C. cylindracea in Mediterranean is seasonal (Ruitton et al. 2005a), with peaks of abundance over short periods (Piazzi et al. 2001b), the recovery of native algae is prevented by the persistence of turfs (Piazzi and Ceccherelli 2006; Klein and Verlaque 2011). Thus, C. cylindracea can ensure monopolization of space by algal turfs and prevent the colonization of native erect algae (Bulleri et al. 2010). Eutrophication The increase in nutrient availability is one of the major causes of biodiversity loss in marine coastal systems (Soltan et al. 2001; Arevalo et al. 2007). Experimental studies have shown that the growth of C. cylindracea on rocky bottom is enhanced under nutrient-enriched conditions (Fig. 1; Gennaro and Piazzi 2011, 2014). Higher values of biomass,
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(B)
high complexity
bare rock
encrusting corallines
total stolon length, frond density and patch size in nutrientenriched areas compared with untreated ones (Fig. 5; Gennaro and Piazzi 2011, 2014) suggest that the competitive ability of C. cylindracea could be enhanced by nutrients (Gennaro and Piazzi 2011). In fact, effects of C. cylindracea on invaded assemblages changed between natural and nutrient-enriched conditions (Gennaro and Piazzi 2011), suggesting the occurrence of a synergistic mechanism between these two stressors. Recently, the intensity and the importance of C. cylindracea competition on resident macroalgal assemblages (intensity and importance being the absolute impact of competition and the relative impact compared to all other influencing factors in the environment, respectively, Welden and Slauson 1986) were evaluated under different levels of nutrient concentrations (Bulleri and Piazzi 2015). Results of the study showed that adding nutrients to the water column did not alter the effect of the intensity of competition of C. cylindracea on species richness, but decreased its importance. In contrast, both the intensity and importance of competition from C. cylindracea on community cover increased following nutrient enrichment. Thus, a greater impact of C. cylindracea under high nutrient levels was not solely the result of increased intensity of competition, suggesting that the importance of competition of C.
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Mar Biol (2016) 163:161 Macroalgal assemblages
16
Seagrass meadow
60
14
50
Percent cover
12
Percent cover
Fig. 3 Mean (+SE) percent cover of Caulerpa cylindracea in canopy macroalgal assemblages (from Bulleri et al. 2010) and seagrass meadow (from Ceccherelli et al. 2014) compared with surfaces where canopy was experimentally removed
161
10 8 6
40 30 20
4 10
2 0
20
80
(A) Patch width (cm)
10
5
0
0
canopy removed
15
Percent cover
Fig. 4 Mean (+SE) percent cover (a) and patch width (b) of Caulerpa cylindracea experimentally transplanted in canopy, encrusting corallines and turf habitats (from Ceccherelli et al. 2002)
canopy present
Canopy
Encrusting
cylindracea depends on the extent to which native species are constrained by biotic interactions versus abiotic factors (Bulleri and Piazzi 2015). A comparative study of tissue nutrient content documented similar response to nutrients and nutritional state of thalli between C. cylindracea and two co-occurring native species (Laurencia chondrioides and Flabellia petiolata). Despite this, only C. cylindracea increased its growth significantly under nutrient enrichment (Gennaro et al. 2015). Thus, the lack of severe nutrient limitation with respect to native algae can explain only partially the success of C. cylindracea invasion in oligotrophic waters of the Mediterranean Sea, as it was instead assumed for other invasive Caulerpales (Delgado et al. 1996). The absence of inhibition in hypertrophic conditions, particularly under high ammonia levels, and quick uptake and reallocation of nutrients along thallus, thanks to the coenocytic structure, are likely the main advantages over the co-occurring species which could in part explain the success of C. cylindracea spread (Gennaro et al. 2015). Eutrophication can enhance C. cylindracea spread also through indirect mechanisms. In fact, nutrient availability also affects the species composition of seaweed assemblages (Teichberg et al. 2008), thereby eroding their natural resistance to invasion. In particular, the increase
Turf
canopy present
canopy removed
(B)
60
40
20
0
Canopy
Encrusting
Turf
in nutrients on rocky reefs is detrimental to slow-growing plants which are adapted to nutrient-poor habitats and creates favorable conditions for faster-growing plants, such as those that compose algal turfs (Gorgula and Connell 2004; Gorman et al. 2009). Turf-forming species are mostly filamentous seaweeds, which generally respond positively to high nutritional availability due to their faster growth, high nutrients requirement and uptake rates (Pedersen and Borum 1997). In summary, eutrophication has a twofold effect on C. cylindracea invasion (Fig. 1), as it promotes the shift from canopy assemblages to algal turfs (Arevalo et al. 2007), thereby triggering positive feedbacks between turf and invasive species described above, and it increases the growth of the invasive alga (Gennaro and Piazzi 2011, 2014). Increased sedimentation Sedimentation in littoral systems is linked to terrestrial sources and can be influenced by human activities increasing the erosion on watersheds and altering the transport of suspended sediments (Airoldi 2003 and references therein). The loss of soil due to overuse of land or deforestation has been recently accelerated, producing a worldwide increase
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70
(A) Biomass (g dry weight m-2)
Fig. 5 Mean (+SE) stolon length (a) and biomass (b) of Caulerpa cylindracea in reference (N−) and enhanced nutrient (N+) conditions (from Gennaro and Piazzi 2014)
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5
Stolon length (m m-2)
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4 3 2 1 0
N-
in water turbidity and sedimentation rates in coastal areas (Airoldi 2003). The interaction between C. cylindracea and sediments has been experimentally investigated, manipulating both sedimentation rates and the presence of the alga (Piazzi et al. 2005a). Results showed that the C. cylindracea is tolerant to high sedimentation rates, as no significant differences in stolon growth were detected among conditions (Piazzi et al. 2005a). This tolerance may depend on resistance to deposition and burial and on vegetative propagation. On the other hand, the deposition of sediment can modify the structure of the bottom facilitating the spread of the alga (Figs. 1, 6; Piazzi et al. 2014; Balata et al. 2015). Moreover, in areas subjected to both C. cylindracea invasion and sedimentation increase, the impact on benthic assemblages was more severe than where the two impacts acted separately, resulting in smaller abundance of the main erect algae (Piazzi et al. 2005a). These results suggest synergistic effects between C. cylindracea and sedimentation. This was also corroborated by the evidence that the amount of sediment in areas invaded by C. cylindracea was seven times higher than that in non-invaded areas (Piazzi et al. 2007b). Thus, C. cylindracea can trap and compact sediments, which become a structural constituent of C. cylindracea populations (Piazzi et al. 2007b). C. cylindracea can overgrow other macroalgae more easily in the presence of a thick sediment layer, as the recruitment of competing species is reduced by the lack of substrate available for spore settlement. Moreover, low redox values were measured in sediment trapped below the mats formed by C. cylindracea, indicating an anoxic environment (Piazzi et al. 2007b). Legacy effects due to trapped sediments within C. cylindracea mats would reduce the recovery of native assemblages even in seasons when the abundance of the alga is low (Piazzi and Ceccherelli 2006) or following its eradication (Bulleri et al. 2010). On the other hand, sediment may also indirectly influence C. cylindracea by enhancing the abundance of algal
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N+
(B)
60 50 40 30 20 10 0
N-
N+
turfs (Fig. 1). Indeed, sedimentation may affect macroalgae increasing water turbidity, inhibiting recruitment, growth and metabolic processes, causing death and removal through burial and scouring (Airoldi 2003; Irving and Connell 2002). Therefore, in high sedimentation areas the structure of macroalgal assemblages shifts, as erect species decline and turf-forming species increase (Airoldi and Cinelli 1997), thus facilitating the spread of the alga (Ceccherelli et al. 2002). Physical destruction of habitats and overfishing Fishing activities and boat anchoring are important causes of mechanical disturbance in marine coastal habitats (Holon et al. 2015). Trawling, in particular, can remove seagrasses or other canopy-forming species and damage bioconstructions (Bordehore et al. 2003; Gonzalez-Correa et al. 2005; Ballesteros 2006). Although to a less extent, also artisanal and recreational fishing activities can damage sensitive organisms (Bavestrello et al. 1997). Fishing activities can affect canopy habitats also indirectly (Fig. 1): depletion of large-sized predators caused by overfishing can determine sea urchins outbreaks (Guidetti and Dulcic 2007; Giakoumi et al. 2012) and, indirectly, promote a shift in dominance from canopy-forming macroalgae to encrusting coralline barrens (Micheli et al. 2005; Gianguzza et al. 2011). Anchoring in sensitive habitats, such as seagrass meadows and coralligenous reefs, is also responsible for canopy loss in many Mediterranean areas (Milazzo et al. 2004; Montefalcone et al. 2006; Ceccherelli et al. 2007; Piazzi et al. 2012). Physical disturbance can negatively affect C. cylindracea colonization, as shown in rock pools (Incera et al. 2010). However, each disturbance damaging or promoting fragmentation of canopy habitats can indirectly facilitate the invasion of the alga. Experimental studies simulating the mechanical destruction of seagrass meadows or stands of erect algae have suggested that removal of
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(A) Biomass (g dry weight m-2)
4
Stolon length (m m-2)
Fig. 6 Mean (+SE) stolon length (a) and biomass (b) of Caulerpa cylindracea in reference (S−) and enhanced sediment (S+) conditions (from Piazzi et al. 2014)
3
2
1
0
S-
canopy habitats enhances C. cylindracea invasion (Ceccherelli et al. 2002; Bulleri et al. 2010; Ceccherelli et al. 2014). However, invasion facilitation may vary in relation to the entity of disturbance, as punctual damaging may be not enough to promote C. cylindracea spread, while wide disturbance or canopy removal in combination with other kinds of disturbance can facilitate the colonization of the alga (Tamburello et al. 2014). The positive relationship between disturbance intensity and invasion success is, however, not universal. For instance, intense disturbance events promoting the dominance of C. compressa, at expense of competitively superior congeneric species (C. barbata and C. crinita), have been shown to enhance resistance to invasion by C. cylindracea (Bulleri et al. 2016). Thus, the net effect of disturbance on invasion success depends on the traits selected within the native species pool and how these relate to those of the invader (Bulleri et al. 2016). The unknown Several abiotic and biotic factors, such as water movement, herbivores and other invaders, have shown contrasting effects on the spread of C. cylindracea. Water movement may enhance the spread of stoloniferous algae such as C. cylindracea through the generation and dispersal of fragments. In fact, propagation through fragmentation is considered an important mechanism of reproduction for Caulerpales (Ceccherelli and Cinelli 1999). Thallus fragmentation can occur either naturally or as consequence of human activity: the former due to wave action in shallow waters and the latter through boat propellers and anchors and fishing. Drifting fragments of C. cylindracea were experimentally dispersed simulating the effects of a storm event: fragments easily established during summer months, independently of the time of detachment from the substrate, suggesting that dispersal by fragmentation is likely to contribute to the wide spread of the alga (Ceccherelli and Piazzi 2001), even if the extent of this
S+
161
(B)
30
20
10
0
S-
S+
mechanism is not known. On the other hand, water movement might limit the spread of C. cylindracea, as the alga is generally more abundant and more persistence through time in sheltered areas (author’s personal observation; Vaselli et al. 2008). Thus, the effects of water movement on the spread of C. cylindracea might be context dependent. Grazing by herbivorous fishes and invertebrates can limit the biomass of C. cylindracea as a variety of native herbivores and omnivores, including fishes and sea urchins, have been found to consume it (Ruitton et al. 2006; Zuljevic et al. 2008; Bulleri et al. 2009; Cebrian et al. 2011; Tomas et al. 2011a, b). In heavily invaded areas, grazing by fish on C. cylindracea may be important, as the alga was found to represent more than 50 % of the fecal pellets of Sarpa salpa (Tomas et al. 2011b) and more than 30 % of the stomach content in Diplodus sargus (Terlizzi et al. 2011). Sea urchins also consume C. cylindracea with variable intensity (Ruitton et al. 2006; Cebrian et al. 2011; Tomas et al. 2011a). Experimental data suggest that grazing can limit the early phases of colonization of C. cylindracea (Caronni et al. 2015), but this factor does not seem able to effectively limit the spread of the alga (Ruitton et al. 2006). In fact, experimental simulation of herbivory suggested that C. cylindracea is able to compensate herbivore effects (Bulleri and Malquori 2015). In fact, growth rates of C. cylindracea increased with the intensity of herbivore-simulated damage, buffering the initial loss of biomass (Bulleri and Malquori 2015). To explain this result, a higher number of growing apices as consequence of stolon fragmentation and a reduction in negative density-dependent effects can be probably advocated (Ruitton et al. 2006). Thanks to the ability to regenerate from remnant fragments of any thallus portion (stolon, rhizoid and frond), C. cylindracea seems able to restore after severe mechanical damage and, hence, it may tolerate intense grazing by native generalist herbivores (Ruitton et al. 2006; Bulleri and Malquori 2015). Moreover, herbivores can indirectly influence the spread of C. cylindracea acting on seaweed and seagrass habitats.
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Experimental studies showed that native herbivores may indirectly facilitate C. cylindracea invasion by reducing the resistance of seagrass meadows (Tamburello et al. 2014). In fact, a reduction in canopy following grazing can allow the alga to penetrate inside the meadow, especially if herbivore activity couples with other kinds of disturbance (Tamburello et al. 2014). The interaction between C. cylindracea and other invasive seaweeds would deserve further investigation. The introduced filamentous Rhodophyta Womersleyella setacea (Hollenberg) R.E. Norris and Acrothamnion preissi (Sonder) Wollaston are the main components of Mediterranean turfs; thus, the presence of some alien algae produces the enhancement of the spread of C. cylindracea (Ceccherelli et al. 2002; Piazzi et al. 2003b; Gennaro and Piazzi 2014). However, C. cylindracea growth was enhanced by the removal of the introduced erect Rhodophyta Asparagopsis taxiformis (Delile) Trevisan, suggesting the occurrence of competitive mechanisms between the two invaders (Tamburello et al. 2013). Also, concerning the competition between C. cylindracea and co-generic invasive algae, transplant experiments showed that C. cylindracea growth was not affected by the presence of C. taxifolia (Vahl) C. Agardh, although the reverse effect was highlighted as C. cylindracea stolons quickly overgrow stolons of C. taxifolia (Piazzi et al. 2001a; Piazzi and Ceccherelli 2002; Piazzi et al. 2003a): whether either allelochemical or overgrowth mechanisms rule this latter interaction still remains unknown. The knowable Although some of the factors regulating the establishment and spread of C. cylindracea have been identified, other aspects are yet to be assessed. The effects of water movement, grazing and interactions with other invasive species need to be investigated in order to improve the information necessary to obtain a complete scenario about mechanisms regulating the spread of C. cylindracea. Although drift of detached fragments has been highlighted to play an important local role in the C. cylindracea colonization, the extent of this mechanism still remains to be investigated to explain geographical patterns of dispersal. Moreover, although negative effects of water movement on C. cylindracea spread have been highlighted, further experimental and large-scale correlative studies are necessary to disentangle the mechanistic interaction between hydrodynamic features and distribution of the alga. Further experimental investigations, possibly involving different guilds of herbivores, are needed to understand their role on the invasion of the alga. The interactions between the relative density of species and the direction and strength of the effects of grazing on resident plant
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assemblages have to be investigated to determine the tradeoffs between negative and positive effects of herbivores on C. cylindracea spread. The occurrence of positive and competitive interactions between C. cylindracea and other algae have been highlighted, but the mechanisms regulating the outcome of the interactions are not known. Further studies should experimentally test the role of both direct competitive mechanisms, such as overgrowth or production of allelochemical substances, and indirect ones through resource exploitation. Human-induced alterations can act concurrently among them and with natural factors creating complex interactions that still have to be studied. Adequate manipulative experiments are needed to investigate effects of multiple humaninduced stressors on C. cylindracea spread and among these latter and biotic and abiotic factors, such as substrate complexity, water movement and herbivores. Finally, although the present overview has identified many factors influencing C. cylindracea dispersal, establishment, growth and competitiveness, their relative strength was not assessed. Specific statistical treatments of data obtained by different correlative and experimental studies are needed to determine the consistency of factors across case studies and their relative importance to promote the successful of C. cylindracea invasion.
Conclusions This overview has allowed the development of a conceptual model based on the known factors influencing C. cylindracea spread. This overview also showed that several aspects have been less investigated or remain unknown, indicating the main goals to reach in further studies. The conceptual model shows the complex interactions among factors influencing C. cylindracea spread. In many cases, feedback mechanisms stabilizing invasion occur, leading to a longer persistence of the invader and to more severe effects on resident assemblages. Furthermore, once C. cylindracea has colonized areas subjected to canopy loss, it is able to prevent the recovery of native populations by facilitating the persistence of alternative assemblages dominated by stress-tolerant species, such as turf ones (Piazzi and Ceccherelli 2006). Thus, the alga seems to have the potential to transform transient ecological effects, generated by a temporary deviation from the original regime of disturbance, into permanent changes (Bulleri et al. 2010). Even if further studies will be necessary to understand the complex mechanisms involved in C. cylindracea spread, patterns emerging from the overview indicate that, irrespective of the relative importance of the different factors involved, the main cause of C. cylindracea spread is the lost of resistance of natural assemblages. Thus,
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conservation of coastal systems represents the only effective instrument to contain the invasion, also because of the weak effectiveness of eradication efforts (Ceccherelli and Piazzi 2005). Thus, protection of canopy habitats and maintenance of good water quality (i.e., prevention of degradation) seem the most effective efforts to enhance the resistance of natural Mediterranean systems against C. cylindracea spread (Piazzi et al. 2005a; Gennaro and Piazzi 2011, 2014; Bulleri et al. 2011; Ceccherelli et al. 2014). C. cylindracea has been one of the most studied marine invaders, and the overall knowledge acquired has allowed the development of the model, here proposed, that describes the interactions among different factors affecting the algal spread. However, the conceptual model may also be useful to study other biological invasions; in fact, any invader spread can potentially be influenced by anthropogenic activities, natural biotic and abiotic factors and by their interactions, whose direction and strength of effects should be estimated. Thus, the proposed model based on measured data may propose hypotheses that proper studies should test for other invasions so that forecasting and responding of ecological effects could be achieved. Acknowledgments L. Piazzi was funded by ‘Desertificazione marina da sovrapascolo di ricci: indagine sulla transizione di stadi stabili bentonici alternativi’ project financed by P.O.R. SARDEGNA F.S.E. 2007–2013—Obiettivo competitività regionale e occupazione, Asse IV Capitale umano, Linea di Attività l.3.1.
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