Conceived and designed the experiments: NS BJS. Performed the experiments: NS. Analyzed the data: NS. Contributed reagents/materials/analysis tools: BJS. Wrote the paper: NS BJS.
The authors have declared that no competing interests exist.
The class Ascidiacea presents fundamental opportunities for research in the fields of development, evolution, ecology, natural products and more. This review provides a comprehensive overview of the current knowledge regarding the global biodiversity of the class Ascidiacea, focusing in their taxonomy, main regions of biodiversity, and distribution patterns. Based on analysis of the literature and the species registered in the online World Register of Marine Species, we assembled a list of 2815 described species. The highest number of species and families is found in the order Aplousobranchia. Didemnidae and Styelidae families have the highest number of species with more than 500 within each group. Sixty percent of described species are colonial. Species richness is highest in tropical regions, where colonial species predominate. In higher latitudes solitary species gradually contribute more to the total species richness. We emphasize the strong association between species richness and sampling efforts, and discuss the risks of invasive species. Our inventory is certainly incomplete as the ascidian fauna in many areas around the world is relatively poorly known, and many new species continue to be discovered and described each year.
Ascidians (Phylum Chordata, Class Ascidiacea), or sea squirts, are the largest and most diverse class of the sub-phylum Tunicata (also known as Urochordata). They comprise approximately 3000 described species found in all marine habitats from shallow water to the deep sea
The name “tunicate” (sub-phylum
Following the original classification of Lahille
a) A simple branchial arrangement in an aplousobranch (
Adult ascidians are sessile, inhabiting a wide variety of habitats such as soft sediments, coral reefs and rocky substrates. They successfully foul various artificial substrata such as jetties, ship hulls, floating docks and other man-made structures all over the world
Both salinity and temperature are among the most important environmental variables influencing ascidian recruitment and reproduction
Ascidians are a key ecological group because of their invasive potential and ability to thrive in eutrophic (nutrient-rich) environments. Introductions of non-indigenous ascidians into harbors in both tropical and temperate waters are now commonplace, with the rate of introductions increasing, sometimes creating severe damage to natural fauna by overgrowth
Ascidians provide a fertile ground for studies in the field of natural products. Similar to sponges and bryozoans, many ascidians avoid predation or fouling by producing noxious secondary metabolites
Ascidians have a poor fossil record
Currently there are numerous web-based sources of taxonomic inventories (e.g., Encyclopedia of Life
Ascidian specimens are held by museums and similar institutions all over the world. However, only a few institutions provide reliable on-line options to search their collections (e.g., Smithsonian Invertebrate Zoology Collections, The Santa Barbara Museum of Natural History, Yale Peabody Museum Catalog Service, The Online Zoological Collections of Australian Museums). In these on-line collections we were able to find invaluable unpublished information regarding species distribution, and verify the occurrence of certain species in their native or introduced range. In addition, a literature search was done to record the number of species identified in various regions of the world in order to provide an estimate of global species richness. It is important to note that the numbers we provide represent the exact number of species mentioned in each citation.
Species distribution information was compiled based on the geographic regions of the Exclusive Economic Zone division v5 standard map provided by VLIZ Maritime Boundaries Geodatabase
We followed the taxonomic classification and used the tabular keys of Monniot et al. 1991
In order to compile a current list of non-indigenous ascidians, we gathered data not only from the available literature but also from different governmental reports which often provide the first record of an introduced species. In addition, valuable information was obtained from the proceedings of the International Invasive Sea Squirt conferences (J Exp Mar Biol Ecol 342 (1), 2007 and Aquat Inv 4 (1) 2009). The list includes only species that are mentioned as introduced or non-indigenous. Species that are classified as “cryptogenic” (species that cannot be reliably demonstrated as being either introduced or native, 68) were not included.
Our systematic list includes 2815 valid species of ascidians. The highest number of species and families is found in the order Aplousobranchia, with approximately 50% of the species (1480) in the class Ascidiacea (
a) Number and percentage of species per order; b) number of species by family within each order.
The discovery rate of ascidian species from 1756 until 2010 is presented in
a) Cumulative number of valid ascidian species described between 1750–2010; b) Percentage and number of species described per taxonomic authority. Note: only taxonomic authorities with more than 100 species are mentioned by name.
Review of the literature resulted in records of 64 non-indigenous species (
Species | Introduced sites | Lifestyle | Order | Remarks | References |
1. |
Netherlands | C | A | NH |
|
2. |
New Zealand | C | A | SH |
|
3. |
Brazil | C | A | SH |
|
4. |
Atlantic Panama | S | P | T, NH |
|
5. |
Mediterranean Sea | S | P | NH | |
6. |
California harbors | S | P | NH | |
7. |
Atlantic Panama, Brazil, Guam, Hawaii, India South America | S | P | T | |
8. |
California harbors | S | P | NH | |
9. |
Argentina, New England, New Zealand, South Africa, South Australia, Tasmania | S | P | ||
10. |
Chile, New Zealand | S | S | SH | |
11. |
California harbors | S | S | NH |
|
12. |
South Australia and Tasmania | C | S | SH | |
13. |
California harbors | C | S | NH | |
14. |
New Zealand | C | S | SH |
|
15. |
Alaska, Atlantic Canada, Belgium, California harbors, England, Mediterranean Sea, Netherlands, New England, San Francisco Bay | C | S | NH | |
16. |
Atlantic Canada, California harbors, India, New England, San Francisco Bay, South Africa, South Australia and Tasmania, US West coast | C | S | ||
17. |
Atlantic Canada, California harbors, Chile, China/Korea, New Zealand, South Africa, South Australia and Tasmania, Washington | S | P | ||
18. |
California harbors, Japana, New Zealand, Washington | S | P | ||
19. |
NW Atlantic, South Africa | C | A | ||
20. |
Brazil | S | S | T, SH |
|
21. |
South Africa | S | S | SH |
|
22. |
Hawaii | S | S | T, NH |
|
23. |
England, Iberia Atlantic coast, New Zealand, NW France | S | P | ||
24. |
Mediterranean Sea | C | A | NH | |
25. |
Atlantic Panama, Brazil | C | A | T | |
26. |
Brazil, Caribbean, Guam, Gulf of Mexico | C | A | T | |
27. |
Hawaii | C | A | T, NH |
|
28. |
England, New England, San Francisco Bay, Washington, widely distributed | C | A | ||
29. |
Brazil, Guam, Netherlands, New England, South Africa | C | A | T | |
30. |
Brazil, Florida, Mediterranean Sea | C | A | T | |
31. |
Brazil | C | A | SH |
|
32. |
Mediterranean Sea | C | P | NH | |
33. |
Mediterranean Sea | C | P | NH | |
34. |
New Zealand | C | A | SH |
|
35. |
India | C | S | NH |
|
36. |
Hawaii, Mediterranean Sea | S | S | T, NH | |
37. |
Atlantic Panama, Hawaii | S | S | T, NH | |
38. |
Guam | C | A | T, NH |
|
39. |
Atlantic Panama, Guam, Hawaii, India, Mediterranean Sea | S | S | T, NH | |
40. |
California harbors, India, Mediterranean Sea, South Africa | S | S | T, NH | |
41. |
Alaska | S | S | NH |
|
42. |
California harbors, Chila | S | S | ||
43. |
California harbors, China/Korea, Europe, NE Pacific, Netherlands, South Australia and Tasmania | S | S | ||
44. |
Atlantic Europe, England, Netherlands, Northern California | C | A | NH | |
45. |
Mediterranean Sea | C | A | ||
46. |
Guam, Hawaii, India, Mediterranean Sea | S | P | T, NH | |
47. |
Brazil | C | S | T, SH |
|
48. |
Hawaii | C | S | T, NH |
|
49. |
California harbors, Gulf of Mexico, Mediterranean Sea | C | S | T, NH | |
50. |
Hawaii | S | S | T, NH |
|
51. |
Brazil | S | S | SH |
|
52. |
Brazil | S | S | T, SH |
|
53. |
Brazil | C | A | SH |
|
54. |
Guam, Brazil, Pacific Mexico | C | A | T | |
55. |
Chile | S | S |
|
|
56. |
Atlantic Panama | S | S | T, NH |
|
57. |
Mediterranean Sea, Florida | S | P | NH | |
58. |
Atlantic Panama, Brazil, California harbors, Guam, India | S | S | T | |
59. |
Atlantic Canada, California harbors, China/Korea, Denmark, England, Germany, Mediterranean Sea, Netherlands, New England, New Zealand, San Francisco Bay, South Australia and Tasmania, England, Washington | S | S | ||
60. |
Brazil, California harbors, China/Korea, Gulf of Mexico, South Africa, South Australia and Tasmania | S | S | T | |
61. |
California harbors, Guam. Hawaii, Mediterranean Sea | C | S | T, NH | |
62. |
California harbors, Hawaii | C | S | T, NH | |
63. |
Brazil, Gulf of Mexico | C | S | T | |
64. |
Mediterranean Sea | C | A | NH |
|
C- Colonial, S- Solitary, Order: A-Aplousobranchia, P-Phlebobranchia, S- Stolidobranchia, Remarks: T- Tropical, NH- Northern Hemisphere only, SH- Southern Hemisphere only.
Records of introduction of ascidians in tropical waters are mainly from Hawaii, Guam and Panama. Of the 64 documented global non-indigenous species, 27 species have records in tropical regions. However, only 14 have records that are restricted to tropical environments (
Area | Number of species | Reference |
Australia | 717 |
|
New Caledonia | 317 |
|
Tasmania | 249 |
|
Mediterranean Sea | 229 |
|
Western Pacific Ocean: Palau, The Philippines, Indonesia, and Papua New Guinea | 187 |
|
South Africa | 168 |
|
Western Mediterranean | 165 |
|
Japan | 163 |
|
New Zealand | 124 |
|
Guam | 117 |
|
Antarctica | 107 |
|
Indo West Pacific region | 102 |
|
French Polynesia | 92 |
|
India | 88 |
|
South America | 87 |
|
Eastern Mediterranean | 86 |
|
Adriatic | 85 |
|
North West Pacific (Kamchatka) | 80 | |
Gulf of Mexico | 70 |
|
Gibraltar | 66 |
|
Iberia | 64 |
|
Fiji | 60 |
|
Pacific Northwest | 60 |
|
Panama | 58 |
|
British | 58 |
|
Timor and Arafura Sea | 57 |
|
Brazil | 56 |
|
Africa north west coast | 55 |
|
Chile | 55 |
|
Scandinavia | 48 |
|
Red Sea | 47 |
|
Hawaii | 45 |
|
California | 45 |
|
Belize | 40 |
|
Jamaica | 39 |
|
Cuba | 39 |
|
Gulf of Saint Lawrence | 37 |
|
Florida | 36 |
|
Hong Kong | 31 |
|
Bermuda | 31 |
|
West indies | 31 |
|
Tanzania | 31 |
|
Mozambique | 29 | |
Circumpolar | 29 |
|
Venezuela | 29 |
|
Massachusetts | 26 |
|
Gulf of Aqaba | 25 | |
Azores Islands | 19 |
|
Galapagos | 16 |
|
Bering Sea | 16 |
|
Bahrain | 15 |
|
Bay of Fundy | 12 |
|
Black Sea | 10 |
|
Data sorted by number of species.
Even though the class Ascidiacea has been the object of much scientific interest in the last decade
In geographical areas where taxonomists have long been active, we typically found high numbers of species. The majority of the described ascidian species (more than 60%) are attributed to only seven taxonomic experts. This is demonstrated in the high species richness found in Australia
The high diversity of some of the ascidian families is remarkable. With approximately 26 families in the class Ascidiacea, the colonial Didemnidae family contains 20% of the described species, possibly due to highly diverse
In general, it has been shown that in tropical environments colonial species dominate the substrate
In temperate waters solitary ascidians comprise 52% of the American fauna
Historical baselines for comparison to present day from museum collections and published literature are required in order to understand and respond to changes in global biodiversity
The majority of records of NIAs are from cold water environments, suggesting this environment may be more favorable to introductions of ascidians. Nonetheless, nearly half of the NIAs have geographical records from tropical environments. Under lab conditions, at high temperature, the growth rate of NIAs was higher compared to that of native species
The class Ascidiacea presents vast opportunities for research in the fields of evolution and development, physiology, natural products, and marine bioinvasion. Yet, there are many areas around the world that are relatively poorly known, and in others the available data should be updated and revised. Many more species are yet to be discovered, contributing to our accumulating knowledge of this unique group.
Systematic division of ascidian species following the Ascidiacea World Database
(DOC)
We express our gratitude to G. Lambert for her advice and helpful suggestions and to C. Primo for her collaboration. N. Shenkar would like to thank the Israeli Taxonomy Initiative and the Dan-David foundation for financial support.