Comprehensive Biometric Study on the Invasive Seaweed, Caulerpa mexicana, in the Aegean Sea

Öz

The present study investigates the occurrence and biometry of the invasive seaweed Caulerpa mexicana in the Gulf of İzmir, Aegean Sea, thereby highlighting its ecological implications in a region increasingly affected by biological invasions. The Mediterranean basin, especially the eastern and Aegean parts, is becoming a hotspot for non-native species, and the region may be a place of interest with the occurrence of the C. mexicana species. This research represents the first detailed assessment of its biometric characteristics in the Levant-Aegean Basin. The study's sampling was conducted from May to August 2024 at 321 stations along the Aegean coast, and C. mexicana was identified at only two specific sites. The species was found in shallow coastal waters at depths of 10 m and 15 m with densities of 630 shoots/m² and 469 shoots/m², respectively. Morphometric analysis revealed frond lengths ranging from 10 to 12.5 centimeters and widths from 7 to 9 millimeters, with a significant correlation between frond length and number of pinnae. Environmental parameters such as temperature, salinity, and dissolved oxygen were measured, providing a context for the species' habitat preferences. The findings underscore the invasive potential of C. mexicana and its capacity to perturb local marine ecosystems, highlighting the necessity for persistent monitoring and management strategies to mitigate its deleterious effects.

Anahtar Kelimeler

• Caulerpa mexicana
• Non-indigenous species
• invasive
• biometry
• Aegean Sea

Ege Denizi'ndeki Istilacı Deniz Yosunu Caulerpa mexicana Hakkında Kapsamlı Biyometrik Çalışma

Öz

Mevcut çalışma, İzmir Körfezi, Ege Denizi'ndeki istilacı deniz yosunu Caulerpa mexicana'nın bulunmasını ve biyometrisini araştırarak, biyolojik istilalardan giderek daha fazla etkilenen bir bölgedeki ekolojik etkilerini vurgulamaktadır. Akdeniz havzası, özellikle doğu ve Ege kesimleri, yerli olmayan türler için bir sıcak nokta haline gelmektedir ve C. mexicana türünün görülmesi ile bölge dikkat çekebilir. Bu araştırma, Ege-Levant Havzası'ndaki biyometrik özelliklerinin ilk ayrıntılı değerlendirmesini temsil etmektedir. Çalışmanın örneklemesi Mayıs-Ağustos 2024 arasında Ege kıyısı boyunca 321 istasyonda yürütülmüş ve C. mexicana yalnızca iki belirli noktada tanımlanmıştır. Tür, sırasıyla 630 sürgün/m² ve 469 sürgün/m² yoğunlukta, 10 m ve 15 m derinlikteki sığ kıyı sularında bulunmuştur. Morfometrik analiz, yaprak uzunluklarının 10 ila 12,5 santimetre ve genişliklerinin 7 ila 9 milimetre arasında değiştiğini ve yaprak uzunluğu ile pinnae sayısı arasında önemli bir korelasyon olduğunu ortaya koydu. Sıcaklık, tuzluluk ve çözünmüş oksijen gibi çevresel parametreler ölçülerek türün habitat tercihleri için bir ilişki sağlandı. Bulgular, C. mexicana türünün istilacı potansiyelini ve yerel deniz ekosistemlerini bozma kapasitesini vurgulayarak, zararlı etkilerini azaltmak için sürekli izleme ve yönetim stratejilerinin gerekliliğini belirtmiştir.

Anahtar Kelimeler

• Caulerpa mexicana
• yerli olmayan tür
• istilacı
• biyometri
• Ege Denizi

Kaynakça

1. Aysel V, Dural B (1998) Türkiye’nin Caulerpaceae Kutz. (Caulerpales, Chlorophyta) üyeleri ve Caulerpa Lamour. Gerçeği. Sualtı Bilim ve Teknolojisi Toplantısı, Bildiriler Kitabı. 15-19 (in Turkish).
2. Benzie JAH, Ballment E, Chisholm JRM, Jaubert JM (2000) Genetic variation in the green alga Caulerpa taxifolia. Aquat Bot 66:131–139
3. Bitar G (1999) Sur les Caulerpa de la côte libanaise (Méditerranée orientale). Actes de l’atelier sur les espèces de Caulerpa invasives en Méditerranée. Heraklion, Crete, Greece, 18-20 March 1998. PNUE, PAM, MED POL. MAP Technical Reports Series, pp. 275-277.
4. Bitar G (2010) La flore marine benthique introduite de la côte libanaise. Etat actuel de trois espèces envahissantes. INOC-Tischreen University, International conference on Biodiversity of the Aquatic Environment, pp. 107-114.
5. Bitar G, Dupuy de la Grandrive R, Foulquié M (2003) Report of the second mission relating to the Development of Marine Protected Areas on Syrian coasts, 1-18 August 2003. Regional Project for the Development of Marine and Coastal Protected Areas in the Mediterranean Region. UNEP, MAP, 40 pp.
6. Bitar G, Ramos-Esplá AA, Ocaña O, Sghaier YR, Forcada A, Valle C, El Shaer H, Verlaque M (2017) Introduced marine macroflora of Lebanon and its distribution on the Levantine coast. Medit Mar Sci 18(1):138–155. https://doi.org/10.12681/mms.1993
7. Catucci E, Scardi M (2020) Modeling Posidonia oceanica shoot density and rhizome primary production. Sci Rep-UK 10:16978. https:// doi. org/ 10. 1038/ s41598- 020- 73722-9
8. Ceccherelli G, Cinelli F (1998) Habitat effect on spatio-temporal variability in size and density of the introduced alga Caulerpa taxifolia. Mar Ecol Prog Ser 163:289–291

9. Ceccherelli G, Cinelli F (1999a) A pilot study of nutrient enriched sediments in a Cymodocea nodosa bed invaded by the introduced alga Caulerpa taxifolia. Bot Mar 42:409–417
10. Ceccherelli G, Cinelli F (1999b) Effects of Posidonia oceanica canopy on Caulerpa taxifolia size in a north-western Mediterranean bay. J Exp Mar Biol Ecol 240:19–36. https:// doi. org/ 10. 1016/ S0022-0981(99) 00044-1
11. Ceccherelli G, Piazzi L (2001) Dispersal of Caulerpa racemosa Fragments in the Mediterranean: Lack of detachment time effect on establishment. Bot Mar 44:209–213. https:// doi. org/ 10. 1515/ BOT.2001. 027
12. Ceccherelli G, Piazzi L, Balata D (2002) Spread of introduced Caulerpa species in macroalgal habitats. J Exp Mar Biol Ecol 280:1–11. https://doi.org/10.1016/ S0022- 0981(02) 00336-2
13. Cevik C, Yokes MB, Cavas M, Erkol LI, Derici OB, Verlaque M (2007) First report of Caulerpa taxifolia (Bryopsidales, Chlorophyta) on the Levantine coast (Turkey, Eastern Mediterranean), Estuar Coast Shelf Sci 74(3): 549-556, https://doi.org/10.1016/j.ecss.2007.05.031.
14. Chisholm JRM, Jaubert JM, Giaccone G (1995) Caulerpa taxifolia in the northwest Mediterranean: introduced species or migrant from the Red Sea?. C. R. Acad. Sci. Paris, Sciences de la vie 318, 1219–1226.
15. Cinar ME, Bilecenoğlu M, Yokeş MB, Ozturk B, Taşkin E, Bakir K, Doğan A, Acik Ş (2021) Current status (as of end of 2020) of marine alien species in Turkey. PLoS ONE 16(5):e0251086. https:// doi. org/ 10. 1371/ journ al. pone. 02510 86
16. Çinar ME, Bilecenoğlu M, Yokeş MB, Güçlüsoy H (2025) Denizel istilacı yabancı tür tanımlama rehberi. MARIAS Projesi, Tarım ve Orman Bakanlığı - Doğa Koruma ve Milli Parklar Genel Müdürlüğü, Ankara, Türkiye. pp 153 (in Turkish).
17. Coppejans E, Tom B (1990) Caulerpa (Chlorophyta, Caulerpales) from the Kenyan coast. Nova Hedwigia 50(1-2):111-125
18. Currie TH, Wing SR, Durante LM (2024) Morphometric and meristic discrimination within juvenile flounder species in New Zealand indicate genetic and environmental disparities. N Z J Mar Freshw Res 1–18. https://doi.org/10.1080/00288330.2024.2314479
19. Duman SG, Mutlu E, Terbıyık Kurt T, Karaca D, Uysal Z (2025) Single station-restricted plankton distribution and Levant occurrence of a copepod, Acartia (Hypoacartia) adriatica with change in P5 as compared to Adriatic and Aegean environments. Cah Biol Mar 66(1):19-37. DOI: 10.21411/CBM.A.353B11D8
20. Erduğan H, Aysel V, Dural B, Akgül R, Balıkçı Ö, Miçoğulları C, Akgül F (2009) A new record for Caulerpa mexicana Sonder ex Kützing from eastern Mediterranean coast of Turkey. J. Black Sea/Mediterranean Environ 15:5-13.
21. Fagerberg WR, Hodges E, Dawes CJ (2010) The Development And Potential Roles Of Cell-Wall Trabeculae In Caulerpa mexicana (Chlorophyta) 1. J Phycol 46(2):309-315.
22. Fagerberg WR, Towle J, Dawes CJ, Böttger A (2012) Bioadhesion In Caulerpa mexicana (Chlorophyta): Rhizoid‐Substrate Adhesion 1. J Phycol 48(2):264-269.
23. Fernandez-Garcia C, Wysor B, Riosmena-Rodriguez R, Pena-Salamanca E, Verbruggen H (2016) DNA-assisted identification of Caulerpa (Caulerpaceae, Chlorophyta) reduces species richness estimates for the Eastern Tropical Pacific. Phytotaxa 252(3):185-204.
24. Gayol P, Falconetti C, Chisholm JRM, Jaubert JM (1995) Metabolic responses of low temperature acclimated Caulerpa taxifolia (Chlorophyta) to rapidly elevated temperature. Bot Mar 38:61–67.
25. Geladakis G, Nikolioudakis N, Koumoundouros George, Somarakis S (2017) Morphometric discrimination of pelagic fish stocks challenged by variation in body condition. ICES J Mar Sci 75(2): 711-718. https://doi.org/10.1093/icesjms/fsx186
26. Gnisci V, Martiis SC, Belmonte A, Micheli C, Piermattei V, Bonamano S, Marcelli M (2020) Assessment of the ecological structure of Posidonia oceanica (L.) Delile on the northern coast of Lazio, Italy (central Tyrrhenian, Mediterranean). Ital Bot 9:1–19. https://doi. org/ 10. 3897/ itali anbot anist.9. 46426
27. Guiry MD, Guiry GM (2024) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway (taxonomic information republished from AlgaeBase with permission of M.D. Guiry). Caulerpa mexicana Sonder ex Kützing, 1849. Accessed through: World Register of Marine Species at: https://www.marinespecies.org/aphia.php?p=taxdetails&id=144468 on 2024-08-06
28. Jongma DN, Campo D, Dattolo E, D’Esposito D, Duchi A, Grewe P, Huisman J, Verlaque M, Yokes MB, Procaccini G (2013) Identity and origin of a slender Caulerpa taxifolia strain introduced into the Mediterranean Sea. Bot Mar 56(1):27-39. https://doi.org/10.1515/bot-2012-01
29. Ljiljana I, Andrej J, Massimo D (2006) Vegetation patterns and spontaneous regression of Caulerpa taxifolia (Vahl) C. Agardh in Malinska (Northern Adriatic, Croatia). Aquat Bot 85:324–330
30. Loos LMvd., Bafort Q, Bosch S, Ballesteros E, B´arbara I, Bercibar E, Blanfun´e A, Bogaert K, Bouckenooghe S, Boudouresque C-F, Brodie J, Cecere E, Díaz-Tapia P, Engelen AH, Gunnarson K, Shabaka SH, Hoffman R, Husa V, Israel A, Karremans M, Knoop J, Gall LL, Maggs CA, Mineur F, Parente M, Perk F, Petrocelli A, Rodríguez-Prieto C, Ruitton S, Sans´on M, Serr˜ao EA, Sfriso A, Sjøtun K, Stiger-Pouvreau V, Surget G, Thibaut T, Tsiamis K, Weghe LVD, Verlaque M, Viard F, Vranken S, Leliaert F, Clerck OD (2023) Non-indigenous seaweeds in the Northeast Atlantic Ocean, the Mediterranean Sea and Macaronesia: a critical synthesis of diversity, spatial and temporal patterns. BioRxiv 2023.06.05.543185. https://doi.org/10.1101/ 2023.06.05.543185.
31. Mayhoub H (1976) Recherches sur la végétation marine de la côte syrienne. Etude expérimentale sur la morphogénèse et le développement de quelques espèces peu connues. PhD Thesis, Caen University, France, 286 pp., 16 pls.
32. Mutlu E (2021) Ecological gradients of epimegafaunal distribution along the sectors of Gulf of İzmir, Aegean Sea. COMU J Mar Sci Fish 4(2):130-158. DOI: 10.46384/jmsf.985685
33. Mutlu E, Akçalı B (2022) Seasonal macro-floral distribution on soft bottoms in a gulf of a metropolitan providence, İzmir, Aegean Sea. Ecological Life Sciences, 17(3):86-103, DOI: 10.12739/NWSA.2022.17.3.5A0168.
34. Mutlu E, Akçalı B, Özvarol Y, Narlı Z, Aslan BE, Zabun Z (2025) Recent plant traits of Caulerpa taxifolia var. distichophylla in the Turkish Aegean Sea. Aquatic Sciences and Engineering, 40(2):63-73. https://doi.org/10.26650/ASE20241574165.
35. Mutlu E, Çağatay IT, Olguner MT, Yilmaz HE (2020) A new sea-nettle from the Eastern Mediterranean Sea: Chrysaora pseudoocellata sp. nov. (Scyphozoa: Pelagiidae). Zootaxa, 4790: 229-244. https://doi.org/10.11646/zootaxa.4790.2.2
36. Mutlu E, Olguner C, Gökoğlu M, Özvarol Y (2022a) Population Dynamics and Ecology of Caulerpa prolifera vs Caulerpa taxifolia var. distichophylla within a Levantine Gulf. Thalassas 38:1311–1325,
37. Mutlu E, Olguner C, Gökoğlu M, Özvarol Y (2022b) Seasonal Growth Dynamics of Posidonia oceanica in a PristineMediterranean Gulf. Ocean Sci J 57:381–397 https://doi.org/10.1007/s12601-022-00078-8
38. Mutlu E, Olguner C, Özvarol Y, Gökoğlu M (2022c) Spatiotemporal biometrics of Cymodocea nodosa in a western Turkish Mediterranean coast. Biologia 77:649–670
39. Olson JL, Valero M, Meusnier I, Boele-Bos S, Stam WT (1998) Mediterranean Caulerpa taxifolia and C. mexicana (Chlorophyta) are not conspecific. J. Phycol. 34:850–856.
40. Paul VJ, Fenical W (1987) Natural products chemistry and chemical defense in tropical marine algae of the phylum Chlorophyta. Bioorg Med Chem 1:1–29. https:// doi. org/ 10. 1007/978-3- 642- 72726-9_1
41. Pereira L (2016) Edible Seaweeds of the World, CRC Press - Taylor & Francis Group, Boca Raton, FL. https://doi.org/10.1201/b19970 (ISBN 9781498730471).
42. Pereira L (2024) Non-indigenous seaweeds in the Iberian Peninsula, Macaronesia Islands (Madeira, Azores, Canary Islands) and Balearic Islands: Biodiversity, ecological impact, invasion dynamics, and potential industrial applications. Algal Res. 78, 103407. https://doi.org/10.1016/j.algal.2024.103407.
43. Rayss T (1941) Sur les Caulerpes de la cote Palesitinienne, Palest. Jour. Bot. Jerusalem, 2: 103-124
44. Robledo D, Yolanda F-P (2005) Seasonal variation in photosynthesis and biochemical composition of Caulerpa spp. (Bryopsidales, Chlorophyta) from the Gulf of Mexico. Phycologia 44(3):312-319, DOI: 10.2216/0031-8884(2005)44[312:SVIPAB]2.0.CO;2
45. Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606. https:// doi. org/10. 2307/ 19417 18
46. Siguan M, Ribera A (2002) Review of non-native marine plants in the Mediterranean Sea. In: E Leppakoski et al. (eds.), Invasive Aquatic Species of Europe, Kluwer Academic Publishers. pp.291–310.
47. Sol D, Maspons J, Vall-Llosera M, Bartomeus I, Garcia-Pena GE, Pinol J, Freckleton RP (2012) Unraveling the life history of successful invaders. Science 337:580–583. https:// doi. org/ 10. 1126/ scien ce.12215 23
48. South GR, N’Yeurt A de R (1993) Contribution to a cataloque of benthic marine algae of Fiji. II. Caulerpa and Caulerpella (Chlorophyta-Caulerpales). Micronesica, 26(2):109-138.
49. Strafella P, Salvalaggio V, Cuicchi C, Punzo E, Santelli A, Colombelli A, Fabi G, Spagnolo A (2021). New geographical record of three cumacean species Eudorella nana, Leucon affinis, Leucon siphonatus and one rare amphipod presence confirmation, Stenothoe bosphorana, in Adriatic Sea, Italy. Thalassas 37:791–801. https://doi.org/10.1007/s41208-021-00294-4
50. Taşkın, E., Evcen, A., Bilgiç, F. (2023) Further expansion of the alien marine green macroalga Caulerpa taxifolia var. distichophylla (Sonder) Verlaque, Huisman & Procacini in Türkiye. J Black Sea/Mediterranean Environ 29(1): 121-126
51. Turan G, Tekogul H, Cirik S, Meinesz A (2011) First record of the invasive green seaweed Caulerpa taxifolia (Bryopsidales) on the coast of Turkey. Cryptogam., Algol 32(4):379-382
52. Tuya F, Martin JA, Luque A (2006) Seasonal cycle of a Cymodocea nodosa seagrass meadow and of the associated ichthyofauna at Playa Dorada (Lanzarote, Canary Islands, eastern Atlantic). Cienc Mar 32(4):695–704. https:// doi. org/ 10. 7773/ cm. v32i4. 1158
53. Uchimura M, Rival A, Nato A, Sandeaux R, Sandeaux J, Baccou JC (2000) Potential use of Cu2+, K+ and Na+ for the destruction of Caulerpa taxifolia: differential effects on photosynthetic parameters. J App Phyc 12:15–23. https:// doi. org/ 10. 1023/A:10081 08531 280
54. Varela-Alvarez E, Gomez Garreta A, Rull Lluch J, Salvador Soler N, Serrao EA, Siguán MAR (2012). Mediterranean species of Caulerpa are polyploid with smaller genomes in the invasive ones. PLoS One, 7(10), e47728.
55. Verlaque M, Ruitton S, Mineur F, Boudouresque CF (2015) CIESM Atlas of exotic in the Mediterranean. Vol.4 Macrophytes [F.Briand ed.]. 364 pages. CIESM Publishers, Monaco.
56. Wright JT (2005) Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations. Mar Biol 147(559):569. https:// doi. org/ 10.1007/ s00227- 005- 1561-5
57. Yelekci O, Ibello V, Fach B, Kucuksezgin F, Yumruktepe C, Sayin E, Salihoglu B, Tugrul S (2021). Assessing the impact of nutrient loads on eutrophication in the semi-enclosed Izmir Bay combining observations and coupled hydrodynamic-ecosystem modelling. Medit Mar Sci 0. https://doi.org/10.12681/mms.23294
58. Zenetos A, Galanidi M (2020) Mediterranean non indigenous species at the start of the 2020s: recent changes. Mar Biodiv Rec 13:10. https:// doi. org/ 10. 1186/ s41200- 020- 00191-4