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3. Invasive Properties, Reproduction & Nutrient Dynamics of C.taxifolia

3.a. Invasive Properties: Reduction in interspecific interactions may also explain why exotic species often flourish in new habitats and become pests. If predators or pathogens of the invasive species are absent in the new community, rapid population growth of the invasive species may occur. Species interactions contribute to the relationship between diversity, food web connectedness, and stability in communities, thus affecting susceptibility of the community to invasion. Furthermore, Spread of invasive species may occur more rapidly in fragmented landscapes, which supports sink populations of native host species, but native species may be unable to persist - except for immigration from outside source populations in more contiguous landscapes (3.6bSakai et al., 2001). An invasive organism is defined as a species that fulfills all of the following criteria (modified after 3.1Carlton, 1985; 3.2Ribera & Boudouresque, 1995; 3.3Williamson & Fitter, 1996; 3.4Boudouresque & Verlaque, 2002).

(i) it colonizes a new area where it was not previously present;
(ii) the extension of its range is linked directly or indirectly to human activity;
(iii) there is a geographical or genetic discontinuity between its native area and the new area (remote dispersal or genetic modification). This means that the occasional advance of a species at the frontiers of its native range (marginal dispersal) is not taken into consideration;
(iv) finally, new generations of the allochthonous species are born in-situ without human assistance, thus constituting self-sustaining populations: the species is established, i.e. naturalized and spreads into new habitats.

The two additional questions which warrant mentioning are:
(i) why do some species become invasive and others not? and also,
(i) is it possible to predict the invasiveness of an introduced species?
Amongst invasive fresh water plants, several common features, likely to account for their success, have been identified (3.5Ashton & Mitchell, 1989; 3.6Pieterse, 1990).

Fig.3 C.taxifolia Simulation3.6a (85kB)

(i) vegetative reproduction is usually the commonest, and often the only method of reproduction; as a result, one viable propagule is sufficient to start a new colony;
(ii) vegetative reproduction is prolific;
(iii) habitat requirements are flexible;
(iv) they tolerate environmental fluctuations and extremes of the invaded habitat;
(v) there is a similarity between the native and recipient habitat;
(vi) they are free from predators and diseases characteristic of their native range;
(vii) human influences aid in the in-/direct proliferation through water pollution, toxicants, etc.

Once initial colonization and establishment have occurred, invasive species may spread from continuing long distance dispersal (saltation dispersal) from foreign sources (naturally or aided by humans) as well as from short-distance dispersal (diffusion dispersal) with lateral expansion of the established population (3.6bSakai et al., 2001). At any given site, this ubiquitous alga is able to colonize most if not all habitats. In the Mediterranean it has invaded Posidonia and Cymodocea seagrass beds, rocks with photophilic or sciaphilic alga, steep cliffs with sponges and sea fans, coarse and muddy sands, with a coverage of up to 100% maintained throughout the year (3.7Vaugelas et al., 1999). Today, more than 90% of the total cover of C.taxifolia is found in the north-western Mediterranean (3.8Meinesz et al. 2001). During the first decade of the Mediterranean invasion, the alga's distribution pattern was rather more irregular and concentrated to zones where heavy development took place or in the vicinity of poorly treated wastewater outlets. The discharge of huge amounts of raw sewage took place till 1981/82, and even as late as 1990, the main sewer outlet for Monaco discharged primary treated wastewater only 400m offshore. This remark is important as wastewater contains large quantities of phosphorous that in turn exhibit extremely low capacities to transform NH4+ into NO2- and NO3- - a fact that can still be found in the geo-chemical signature of the sediments (3.9Chisholm et al., 1997).
With the regression of the once abundant autochthonous flora (P.oceanica meadows, 3.10Olivier, 1929) that started some 30 years before the invasion of C.taxifolia took off, it was an ideal hub for C.taxifolia's to invade the N-W Mediterranean (3.11Meinesz and Laurent 1978; 3.12Falconetti and Meinesz 1989; 3.13Chisholm et al., 1997).

Analysis in that area have revealed that total organic material, i.e. including size fractions of decayed seagrass leaves, rhizomes and raciness of P.oceanica (>2mm), was high in all sediments providing excellent conditions for C.taxifolia growth. Concentrations of non-crystalline sulfide were high in all potential locations. With the Ligurian Current flowing from east to west along the north Mediterranean coast and along with it contaminants traveling huge distances from their site of origin, it is therefore not coincidental that C.taxifolia has invariably begun proliferating around the periphery of headlands (3.14Meinesz et al. 1994), which are both zones of current impaction and favored sites for wastewater discharge (3.9Chisholm et al., 1997).

Fig.3.a Underwater sewage outlet (50kB)

Since the launch of the invasion in 1984, the alga's spread continued resulting in coverage indices in the most affected benthic areas of up to 100% between depths of 1 to 35m. Below this depth, it has been observed - though at much smaller densities - as far down as 100m (3.15Belsher & Meinesz, 1995). Such depths are unknown for the tropical strain of C.taxifolia: 30m at Papua-New Guinea, 32m at Tahiti, 50m at New Caledonia, 32m in the tropical Atlantic around Virgin Islands, St. Croix (3.15Belsher & Meinesz, 1995).
Being of tropical origin, the frequently adopted thought that a 12h tropical day converts to a 12hr irradiance under water is incorrect, since the rays are reflected both at dawn and dusk beyond the angle of total reflection. Taylor (3.14a,1960) and Larcher (3.14b,1995) report that photosynthesis comes to a halt at peak illumination times during the tropical day, further shortening the duration of effective irradiance to 7-9 hours per day. Hence very little sunlight penetrates the water surface during these hours that make the Mediterranean and similar temperate oceanic regimes ideally adapted for its proliferation.
Another adaptive property of this aquarium strain, when growing in shallow coastal waters, is its capacity to prevent total desiccation; i.e it simply grows among algae that are structurally better capable of maintaining their water content. This leads to another stunning attribute of C.taxifolia: it can survive out of water and under humid conditions, for up to 10days (3.16Sant et al., 1994). Thus floating debris, that are washed up on the beach during low tide, can survive a long enough period until high tide carries the mat back out to sea.
A further feature of this invasive species is its habitat tolerance; it can florish in a wide variety of substrates, including sandy bottoms, rocky outcroppings, mud, sheltered bays, natural meadows (overgrowing flora), suffocating sessile fauna and does not even refrain from artificial substrates (concrete jetties, metal buoys rubber bumpers, car tires that are used to protect ships, pipes, plastic lines, ship and nylon ropes; 3.20bDebelius & Baensch, 1997). As will be discussed further below, C.taxifolia is able to withstand severe nutrient limitation (3.17Delgado et al., 1996). On top of that, the algae adapts to any milieu, be it a polluted port or a clean, isolated bay. This explains why C.taxifolia flourishes in nutrient rich water (predom. ammonia and nitrate) of marine aquaria to such a degree that large quantities can be harvested and removed (3.20bDebelius & Baensch, 1997).

Potential invasion sites are first colonized around headlands and were drifting algal fragments can attach. With its ability to form dense carpets, the aquarium strain is capable of extremely rapid growth resulting in exceptionally dense meadows. This is in sharp contrast to the tropical strain of C.taxifolia where it occurs in isolated and patchy aggregations (3.18Meinesz & Hesse, 1991).
So far the aquarium strain has not been found, where water temperatures fall below 20C. Yet, it has been shown that the alien version of this plant can survive in the laboratory at temperatures of 10C for three months (its lethal threshold value is at 7C). In the Mediterranean, where winter temperatures generally drop to just 13C these algae maintains its dense underwater meadows - despite signs of chlorosis (3.19Gnassia-Barelli et al., 1995).
During summer (June to September) the thallus of the aquarium alga attains extreme growth rates of up to 32mm of new stolon per day and a new frond every other day (month of August) resulting in frond densities of approximately 5000 fronds/m2 (3.20Meinesz, 1995). An extremely densely covered single square meter of seafloor can be matted with 230m of stolons, from which emerge up to 8000 leafy fronds (3.18Meinesz & Hesse, 1991).

Fig.3.b Invasive properties of C.taxifolia (105kB)

Fig.3.c meadows of C.taxifolia (140kB)

Niel (3.18a,1983) mentions that C.taxifolia (as well as C.sertularioides) shades itself by widening the tips of their fronds (which are normally finely pinnulate), while the rhizoids remain cooly encased in the mud. Both two species have ecological variations, but it seems questionable whether this is a consequence of solely temperature, since different ecological variations seem to have different allowable temperature ranges. It is possible though, that this depends on the environment that this species is adapted to. There seems to be a positive correlation in that lush plant growth is a function of intense irradiance and high water temperature (3.20bDebelius & Baensch, 1997).
Thus it comes of no surprise that C.taxifolia growing in the Mediterranean sea (with distinct seasons such as summer and winter) exhibits a corresponding growth rhythm. New sprouts emerge in the spring from the remnants of the overwintering population. These plants can grow 1-2cm per week (growth in the tropics is much faster). However, this rapid growth is matched by rapid aging; i.e. the oldest part of the colony dies as the newer sections continue to creep. Usually, the difference between decay at the back and growth at the front is 6-14 weeks and is related to temperature and available nutrients (3.20bDebelius & Baensch, 1997). Although large-scale die-off occur in shallow waters (0.52 m), in most waterways during the cooler months and particularly after heavy rainfall (compare fig.1.f - Chapter-1, 3.20aCreese et al., 2004), this die-back as a result of decreased temperatures, lower salinity and increased turbidity, is only temporary as the algae picks of again during the warmer months to make up lost ground and to proliferate beyond pre-established limits. Thus, the rate of expansion of this invading species as well as the impacts noted upon the environment, along with the feature of asexual reproduction that will be discussed shortly, assigns this weedy species a catastrophic and property represents a major risk for shallow underwater ecosystems of the Mediterranean.

3.b. Reproduction: Like many plants and virtually all algae, species of the genus Caulerpa can reproduce both sexually and asexually (3.20bDebelius & Baensch, 1997). In the case of the aquarium strain of C.taxifolia only male gametes have been observed and this strain is apparently only vegetatively spreading (3.21Zuljevic and Antolic, 2000). Sexual reproduction of this aquarium strain appears to be a stochastic event (Clifton and Clifton, 1999) as it has been only observed in temperatures above 25C (3.21Zuljevic and Antolic, 2000). Nonetheless, C.taxifolia corresponds to most of the characteristics common to successful colonists across taxa; i.e. r-selected life histories (use of pioneer habit, short generation time, high fecundity, and high growth rates) and the ability to shift between r- and K-selected strategies (3.21a, Sakai et al, 2001).

Caulerpa's life cycle is therefore poorly understood. Most siphonous green algae are primarily diploid; the gametes are the only haploid cells in the life cycle (3.24Raven et al., 1992). Due to its siphonous nature, no cross-walls are present, housing multinucleated cells (coenocytic) packed with chloroplasts. So when sexual reproduction does occur, the individual nuclei undergo meiosis. This yields 4 gametes for every nucleus, which are separated by cell walls (fig.3.d). Hence, this process involves "holocarpy", in which the entire protoplasm gives rise to gametes at once; i.e. almost all of the protoplast of a thallus is converted into gametangia containing biflagellate dissimilar (anisogamy), motile gametes, which are discharged simultaneously through papillae. Upon merger of the gametes, the zygote develops into a protonema, which then forms a typical diploid (2n) thallus (3.23Silva, 2002). Since C.taxifolia's life cycle is poorly understood, it could well be that the mature sporophyte releasing quadri-flagellated zoospores that in turn would give rise to the gametophyte (n), is inexistent (see fig.3.d).
According to Meinesz, C.taxifolia is able to disperse a shower of male and female gametes that pair up and fuse to form a zygote (new plant) under lab-conditions. But over more than 10 years that he has observed this species in the Med and in the lab, he has never seen evidence of sexual reproduction. In the wild, though, the only reproductive cells released are male (fig.3.e), confirming existing evidence that all C.taxifolia in the Mediterranean are clones of that single aquarium plant release in 1984.
Genetically, this invasive species shows relatively little variation, thus vegetative reproduction by fragmentation is the most common mode of proliferation (asexual or clonal propagation). The break-up of thalli (mediated via anchor damage, fishing gear or storm activity as small as 1cm2) gives rise to new colonies that usually appear in 2 to 10m deep water (3.25Meinesz et al., 1993) during summer and fall when growth rates are highest (compare fig.5.f of Chapter 5).

Fig.3.d Lifecycle of C.taxifolia (75kB)

Fig.3.e Gametes of C.taxifolia (55kB)

Fig.3.f Vegetative reproduction of C.taxifolia (95kB)

3.c. Nutrient dynamics: Little is known about the nutrient dynamics of C.taxifolia such as its preferred high affinity for nutrients, its ability to take up nutrients from the sediments via rhizoids, and its capacity to store nutrients. Studies on other members of Caulerpales suggest the existence of some of these features. C.taxifolia can utilize nutrients and carbon sources from the sediment via uptake through the rhizoids and associated bacteria (Chisholm et al., 1996), even in eutrophicated, anoxic sediments (3.26Chisholm and Jaubert, 1997). Therefore the alga was shown to be tolerant to shading conditions (3.27Komatsu et al., 1997) enabling growth in areas where photosynthesis is light-limited as a result of greater depths or during the darker winter months.
As mentioned above, enrichment of sediment with inorganic components originating from wastewater discharges, are some of the prerequisites for the alga's success in the N-W Mediterranean. This assumption was confirmed by recent studies indicating that C.taxifolia only succeeds in colonization sparse or patchy P.oceanica communities (3.28deVillele & Verlaque, 1995). Once C.taxifolia proliferates due to the heavily enriched inorganic material perfused with hydrogen sulfide, it alters the sediment's "microclimate" into anoxic conditions (see fig.3.g). These are usually conditions that kill most autochthonous algal species that have been tested in studies on algal mats in eutrophicated waters (3.29Schramm & Both, 1981). When there is no growth of fronds (winter) and photosynthesis is weak (>30m), copper, iron, manganese, and lead concentrations were high, indicating an adsorption process from the substrate for uptake (3.30Gnassia-Barelli et al., 1995). These observation are in line with those documented by Debelius & Baensch (3.20b,1997) who write that nutrients such as cobalt (Co) copper (Cu), iodine (I), iron (Fe), manganese (Mn), nitrate (NO3-), phosphate (PO4=), vanadium (V), zinc, (Zn) re-establish growth. Take up of these substances is facilitated via the excretion of metabolites that chelate metals, making them soluble and available to C.taxifolia. On the other hand, Caulerpa is also capable of returning a large percentage of its absorbed substances to the environment - especially during the die-off periods of the cooler season.

Field observations revealed that floating fragments of C.taxifolia (even under intense irradiance) render the algae looser, longer, and more flaccid compared to the same species attached, benthic samples, indicating that rhizoids are more than merely anchoring organs. Rhizoidal filaments can enter deep into the porous substrate and adhere to grains of sand. Research on rhizoids showed that they contain many storage compounds such as amylum (starch) (3.20bDebelius & Baensch, 1997). This is in line with laboratory studies, which have shown that sediments containing decaying organic matter of out-competed sea grass turn black in color once penetrated by the rhizoids of C.taxifolia (fig.3.g). The change in coloration is the result of redox conditions (bacterial reduction of sulfate to sulfide) favoring N2-fixation, thus enhancing nutrient supply to the alga's rhizoids. In addition, and apart from the rhizoid's capability to effectively utilize nitrogen products produced by anaerobic bacteria, C.taxifolia appears to activate the fermenting bacterial community by releasing photosynthetic product from its rhizoids in the form of simple sugars into the rhizosphere - similar to salt marsh and sea grasses. A process that can be simulated by simply injecting solutions of glucose or sucrose into unvegetated sediments (3.13Chisholm et al., 2003). C.taxifolia's success thus stems from its ability to produce organic and inorganic nutrients from sediments via endocellular bacteria that potentially facilitate removal of toxic sulphide (3.31Chisholm et al., 1996). The bacterial community fertilized and cultivated in this way combined with the antifouling properties of the algae, are key elements in rendering the substrate so hostile to other biota. These facts are underlined by observations made in the tropics (i.e. those found along the coast of central Java, Indonesia) where this algae engages in some sort of environmental "shaping" in that dense stands "accumulate" substantial amounts of mud. This may seem unexpected, particularly when seen in such crystal clear waters, and is yet further evidence that it creates its own nutrient reservoir by trapping and accumulating debris of any kind, which in turn is an excellent substrate to colonize bacteria that are highly beneficial for its development. (3.20bDebelius & Baensch, 1997).

Fig.3.g Rhizosphere and rhizomes of C.taxifolia (100kB)

Chisholm's data indicate that the growth of C.taxifolia substantially enhances nitrogen production in high C:N sediments on dead Posidonia sediments in relatively low-nutrient seawater, thus facilitating organic matter turnover. C.taxifolia's ability to stimulate nutrient turnover in substrata and then take up a proportion of the resulting nutrients via its subterranean rhizoids likely assists the remediation of sediments that are burdened by large quantities of refractory organic waste (3.32Chisholm & Moulin, 2003).
The same authors though predict that heterotrophic bacteria are the primary beneficiaries of N2 fixation, thereby re-mineralizing C, N, and P. Once the transformation of the sediment's eutrophicated organic matter approaches completion, the abundance of C.taxifolia should decrease dramatically in the absence of an exogenous N supply of similar magnitude. This might explain some of the many boom-bust cycles of Caulerpa growth that have occurred in different environments (3.33LaPointe et al. 1994; 3.34Panayotidis & Montesanto, 1994; 3.35Doumenge 1995; 3.36Davis et al., 1997). As the spread of Caulerpa might reach a plateau - be it by nutrient shortage or natural regulation (via a yet unknown predator - compare Chapter 5) the pollution prevention of marine habitats with wastewater, are just a few of a series of steps necessary to halt its hunger for new territories.
At 10m depth, the persistently high biomass of C.taxifolia in dense meadows of up to 613g/m2 dry-weight (according to Verlaque & Fritayre (1994), which corresponds to a fresh-weight biomass of approx. 4kg/m2 or more) represent an important nutrient trap, holding about 1g phosphorous/m2 and 14g nitrogen/m2. During summer and autumn when fronds of this alga reach their maximum length of 60-80cm, the biomass of C.taxifolia can exceed 10kg wet weight/m2 (3.18Meinesz and Hesse, 1991; 3.38DeVillle & Verlaque, 1995).
These data are two-fold higher than the phosphorous contained in a seagrass bed of P.oceanica, though frequently lower than the amount estimated for populations of sublittoral algae (3.20Meinesz et al., 1995). In this regard, the siphonaceous nature of the thallus of C.taxifolia facilitates the nutrient translocation of the stored nutrients, as well as the reallocation of nutrients taken up from either the water column or the sediment. Likewise, nutrient recycling inside C.taxifolia meadows may have a pre-enrichment role in nutrient availability to the plant through nutrient reabsorption from dead and decomposing parts excreted by resident animals and bacterial activities.

In response to changes in light, temperature and nutrients, most of the Mediterranean seaweeds and sea-grasses have distinct annual cycles of biomass accretion and productivity. In fact this alga has a very low light compensation point and can grow in low light levels (3.39Garcia et al., 1996; 3.26Komatsu et al., 1997). Most of the dominant seaweeds and sea-grasses in the Mediterranean display their lowest biomass gain and productivities during fall (3.40Ott, 1980, 3.41Bay 1984, 3.42, 43Ballesteros, 1989 & 1992). In contrast C.taxifolia displays the highest photosynthesis activity in November, coupled with large thalli dimensions (3.28Villele & Verlaque, 1995). Since C.taxifolia is a pseudo-perennial the high photosynthetic capacity during fall provides a competitive advantage to C.taxifolia over other species. Fig.3.h shows the short-term effects of temperature on light saturated photosynthesis (net productivity) and dark respiration rates of C.taxifolia collected in summer July '93 and winter Jannuary'94 (left). The right half shows the photosynthetic rates as a function of photon flux density for plants of organic dry weight of C.taxifolia collected at various times of the year from 9m depth at Cap Martin (France) (3.39Garcia et al., 1996).

Fig.3.h Effects of light and temperature on growth rate of C.taxifolia (75kB)

Although this species is pseudo-perennial (3.20Meinesz et al., 1995), the aquarium strain of C.taxifolia can resist hard winters showing vigority not present in its tropical counterpart. The aquarium hybrid prefers cooler water (around 10C); its lethal minimum temperature in the Mediterranean is 7C, lethal minimum temperature elsewhere is 14C (3.27Komatsu et al., 1997); optimum growth temperature is 20-30C; its lethal maximum temperature is 32C. The year-round biomass accumulation of C.taxifolia has been estimated to average 5.5kg/m2 (fresh-weight at Cap Martin, 3.20Meinesz et al. 1995). Such production translates to a dry weight increase of 7.03gm-2d-1 using a mean organic C to total dry weight ratio of 1.757:1 (3.39Garcia et al., 1996). In addition, sediment nutrient enrichment has been shown to increase growth of Mediterranean C.taxifolia (3.44Ceccherelli & Cinelli, 1997). Together all these features explain its outstanding growth ability and out-competing properties towards autochthonous species.

Please continue with PART-IV - Effects of C.taxifolia on autochthonous species and C.taxifolia's toxicity