Occurrence of the introduced alga Caulerpa ollivieri Dostál , 1929 ( Caulerpaceae , Chlorophyta ) in the Southern Gulf of Mexico

This work reports the occurrence of the introduced alga Caulerpa ollivieri Dostál, 1929 in the Southern Gulf of Mexico off the northern coast of the Yucatan Peninsula, Mexico. In 2010, a specimen was collected off the Dzilam de Bravo, and additional specimens were detected in at least four localities along the coast. These records extend the distribution of C. ollivieri 800 km to the south; it was first recorded off the Tampa Bay in Florida (USA) in 1968 and subsequently in The Bahamas. Further work is now needed to determine the impact this introduced alga may have on the native benthic community.

Caulerpa ollivieri Dostál, 1929 is an alga native to the Mediterranean Sea that was found in the northern Gulf of Mexico, but treated as a form of C. prolifera (Forsskål) J.V. Lamouroux, 1809 (Dawes and van Breedveld 1969).However, Hine and Humm (1971) recorded C. ollivieri as a valid species for the first time in the Gulf of Mexico, close to the mouth of Tampa Bay in Florida where it was detected at a depth of 30 m.Recently, Lapointe et al. (2005) recognized C. ollivieri as an invasive alga in the harbors of The Bahamas.

Methods
The study area extends from Las Coloradas (21°38'55.29"N;88°04'0.83"W) to Sisal (21°12' 35.3"N; 90°04'04.65"W)(Figure 1) off the northern coast of the Yucatan Peninsula.From 2010 to 2013, six sampling locations (3 to 10 m deep) in total were surveyed using SCUBA.Caulerpa ollivieri was detected during benthic surveys that targeted other macroalgae groups in the area.About five to six specimens of C. ollivieri were collected opportunistically directly from the bottom in each locality; however, no data on cover or density were recorded.Specimens were fixed in a solution of 4% formalin in seawater.In the laboratory, they were measured in millimeters and identified following Dawes and Mathieson (2008).Morphological characters measured included: fronds (width and length), stolon (length and diameter), rhizoidal pillars (diameter), secondary rhizoidal pillars (diameter), rhizoidal (diameter), and rhizoidal bouquets (diameter) (Kluser et al. 2004).Specimens were pressed dry and deposited in the Herbarium "Alfredo Barrera Marin" from the Universidad Autónoma de Yucatán (UADY), in Mérida Yucatán, México.

Results and discussion
During the summer in 2010, Caulerpa ollivierii was detected off the Dzilam de Bravo coast of the Yucatan Peninsula (21°29'50.37"N;88°44' 17.96"W) in a low visibility area in water 10 m deep.Three specimens were collected, preserved, and brought to the laboratory where it was identified and deposited in the herbarium (UADY 1037).More specimens were collected off the north coast of the Yucatan Peninsula in 2013, as well as in other locations (Las Coloradas, Rio Lagartos, Telchac, Progreso and Sisal), at depths of 3 to 10 m (Figure 1, Appendix 1).All collected specimens were stoloniferous, with stolons 50 mm long (0.34-0.38 mm wide), and erect fronds up to 70-78 mm high (3.9-4.2 mm wide) (Table 1).Thalli grew over a sandy bottom with poorly developed rhizoids (0.26-0.28 mm diameter) that were infrequently branched.Blade proliferations emerged from the lower midlines of the blades (Figure 2).Specimens of C. ollivieri were part of an algal mat (turf) that mainly consisted of other species of Caulerpa (e.g., C. microphysa Weber-van Bosse) Feldman, 1855 and C. paspaloides (Bory de Saint-Vincent) Greville, 1830), but with C. ollivieri as the primary species.In the turf there were also red algae, such as: Jania adhaerens J.V. Lamouroux, 1816; Amphiroa fragilissima (Linnaeus) J.V. Lamouroux, 1816; Hypnea musciformis (Wulfen) J.V. Lamouroux, 1813; and H. spinella (C.Agardh) Kützing, 1847.The turf was 5 and 10 cm high and growing on a thin layer of sand (< 5 cm thick) with patches of bare rock colonized by calcareous and stoloniferous species (Figure 3).
The specimens of C. ollivieri from the Yucatan Peninsula were, morphologically, slightly different from those described from Florida (Hine and Humm   1971).The Yucatan specimens had a lower density of rhizoids and grew obliquely upwards from a small attachment area where the stolons develop fibrous holdfasts, which is a characteristic of Caulerpa.In contrast, the specimen from Florida had proliferations of erect branches developing from the apices, apparently in response to low light intensity (Hine and Humm 1971).We think C. ollivieri is widely distributed on the north coast of the Yucatan Peninsula, and assume that it has established permanent populations in the area.Our account extends the C. ollivieri distribution about 800 km south to the Gulf of Mexico from where it was first recorded off the Tampa Bay in Florida, USA.In addition, this is the first record for Mexico of C. ollivieri.In general, Caulerpa species are capable of spreading rapidly over large areas and creating turfs (Williams 2007).In The Bahamas, for instance, C. ollivieri can replace the seagrass Thalassia testudinum Banks ex König, 1805 in eutrophic coastal waters (Lapointe et al. 2005).Any stress directly or indirectly reducing seagrass density may contribute to increasing seagrass susceptibility to replacement by introduced macroalgae species (Williams 2007).
How C. ollivieri was introduced to the waters of the Yucatan Peninsula is unknow; however, it could have been introduced via ballast water of cruise ships coming from the USA to Progreso port.However, there is no evidence to support this hypothesis.In the Yucatan, C. ollivieri was detected in relatively small patches in seagrass.Environmental parameters were not recorded, but there are no urban developments in the area where the specimens were detected; consequently, sewage input to the area is minimal.We currently do not know how C. ollivieri is affecting the native benthic community, especially the seagrass beds, but further work is warranted to track population trends and the consequences of spread of this non-native species to this coastal ecosystem.

Figure 1 .
Figure 1.Map of study area in the Southern Gulf of Mexico along the northern Yucatan Peninsula, Mexico, showing sites where Caulerpa ollivieri was detected.

Figure 2 .
Figure 2. Caulerpa ollivieri from the southern Gulf of Mexico off the northern Yucatan Peninsula in Mexico.Photo by I. Ortegon-Aznar.

Table 1 .
Morphological characters of Caulerpa ollivieri from the northern Yucatan Peninsula, Mexico.