The barnacle Amphibalanus improvisus ( Darwin , 1854 ) , and the mitten crab Eriocheir : one invasive species getting off on another !

The balanoid barnacle, Amphibalanus improvisus (Darwin, 1854), was found on the carapaces of two invasive species of mitten crabs: Eriocheir sinensis H. Milne Edwards, 1853 and E. hepuensis Dai, 1991. The first instance was from a female mitten crab captured from the River Thames estuary, Kent, England, where A. improvisus is common. However, the second record, on a Hepu mitten crab from Iraq is the first record of A. improvisus from the Persian Gulf.


Introduction
"Hairy" (Southeast and East Asia) or "mitten" (Europe) crabs are currently assigned to Eriocheir De Haan, 1835 (Brachyura: Grapsoidea: Varunidae).These crabs are catadromous spending most of their life (four to five years) in freshwater, but migrating to higher salinity water to reproduce and for the females to hatch zoea larvae (Panning 1939;Clark et al. 1998;Naser et al. 2012).After the mating period, the adults die off (semelparous), and the juveniles migrate upstream to start the life cycle again.Reproductive adult crabs do not moult during their ca.8-10 months in higher salinity and, consequently, their carapaces can become fouled with barnacles (Figures 1, 2).
The barnacle Amphibalanus improvisus (Darwin, 1854) is considered native to the eastern coasts of the Americas, but this species was known to Darwin (1854) from both sides of the Atlantic, and from the Pacific in tropical South America.The present distribution of A. improvisus includes: the eastern and western North Atlantic; Baltic Sea; west coast of Africa (to the Cape of Good Hope); Mediterranean Sea; Black Sea; Caspian Sea; Red Sea; Straits of Malacca; Singapore; Australia; New Zealand; China; Bohai Sea; Japan; Pacific coast of USA from Washington to San Francisco; Mexico; Columbia; Ecuador; and Peru.Amphibalanus improvisus continues to spread through vessel fouling (Jones 1991(Jones , 1992(Jones , 2012;;Leppäkoski 1999;Olenin 2006).
In its native and invasive ranges, A. improvisus occurs from the littoral to the shallow subtidal being found in mesohaline regions of estuaries world-wide, but it is euryhaline and tolerates brackish to fully marine waters.The species attaches to hard substrates including rocks and wood, and also fouls animate surfaces, e.g.macroalgae, crustaceans and molluscs (Olenin 2006).It also fouls artificial hard surfaces such as ships' hulls, dock and bridge pylons, and other marine infrastructures (Leppäkoski et al. 2002;Katsanevakis et al. 2014).In this study, we document the balanoid barnacle, Amphibalanus improvisus (Darwin, 1854) attached to the carapaces of Eriocheir sinensis H. Milne Edwards, 1853 collected from the estuary of the River Thames, London, England, and on E. hepuensis Dai, 1991 collected from the Shatt Al-Basrah canal, Iraq.The latter represents a first record of A. improvisus for the Persian Gulf.

Collection of specimens and diagnosis
Specimens of mitten crabs carrying barnacles were collected opportunistically.Each was measured (carapace width × length in millimetres) and barnacles collected and identified to species.The specimens of Amphibalanus collected in the present study were identified using Henry and McLaughlin (1975).They were compared to all other Amphibalanus species that could be expected to occur in the area: A. amphitrite (Darwin, 1854); A. eburneus (Gould, 1841); A. improvisus, A. subaldidus (Henry, 1973); and A. venustus (Darwin, 1854).Five distinguishing features were examined (Table 1).

Discussion
To date, 43 thoracican barnacles species are known from the waters of the Persian Gulf (33 species) and the Gulf of Oman (26 species) (Shahdadi et al. 2014).Records indicate that three amphibalanine balanids (Amphibalanus amphitrite, A. subaldidus and A. venustus) are recorded from these waters.All three species are considered to be foulers: two species are cryptogenic and one is regarded as an introduction.Amphibalanus amphitrite is a cryptogenic, cosmopolitan species that is recorded from the Persian Gulf by Nilsson-Cantell (1938, as Balanus amphitrite hawaiiensis Broch, 1922, locality unknown); Stubbings (1961, as Balanus amphitrite var. communis Darwin, 1854; and Balanus amphitrite var.hawaiiensis, from Kuwait); Utinomi (1969, as Balanus amphitrite, from Hormoz Island); Jones (1986, as Balanus amphitrite var.communis, from Kuwait); and Shahdadi et al. (2014, as Amphibalanus amphitrite, from various localities along the Iranian coast, salinities ranging from 5-43 psu).The species is also recorded from the Gulf of Oman by Utinomi (1969, as Balanus amphitrite, locality unknown); and Shahdadi et al. (2014, as Amphibalanus amphitrite, from various localities along the Iranian coast).
Although Amphibalanus subaldidus has not been recorded from the Gulf of Oman, it was recorded for the first time along all river banks in the northern Persian Gulf, from a variety of animate and inanimate substrates by Shahdadi et al. (2014), as Amphibalanus subaldidus, from the Arvandroud River (salinity 17.8), the Karoon River (salinity1.6), the Bahmanshir River, and the Zohre River.The native range of this species is the Western Atlantic Ocean and Gulf of Mexico (Henry and McLaughlin 1975); therefore, A. subaldidus is considered to be an introduction into the waters of the Persian Gulf.
Herein, we present the first record of the Atlantic brackish-water species, Amphibalanus improvisus from the Persian Gulf thus bringing the number of amphibalanines known from this area to four.
Amphibalanus improvisus is now recognized as a widely distributed species, indicating its ability to become established in warm temperate to tropical regions of the world.The species is recognized as a nuisance fouler in estuaries, and is reported to have a high impact on ecosystem services and biodiversity (Leppäkoski 1999;Zaiko et al. 2007;Katsanevakis et al. 2014).Vulnerable habitats are brackish water bays and estuaries to shallow marine habitats (to ~6 m depth).Such foulers have the propensity for habitat modification and harmful impacts on other biota through competition for space and food resources, including on commercial species (e.g., fouling of mussels and oysters in aquaculture cages).They can also be harmful to human health, for example by fouling water intake pipes and heat exchangers.As well, the fouling of boat and ships' hulls and man-made constructions, such navigational constructions, breakwaters, etc., impacts highly on transport efficiency.
High marine traffic is experienced in the Persian Gulf due to oil-related industries.The northern part of the Gulf has the highest number of oil terminals and the largest ports, with an estimated 25,000 tankers transporting crude oil across the Strait of Hormuz annually (Haapkylai et al. 2007;Shahdadi et al. 2014).Barnacles are known to successfully cross biological barriers as hull foulers or via ballast water (Yamaguchi et al. 2009;Tottrup et al. 2010).Therefore, with high ship traffic, the area is vulnerable to establishment of alien invasive marine species (Naser et al. 2012).
Recently, Shahdadi et al. (2014) reported the introduction and establishment of Amphibalanus subaldidus in the Persian Gulf, in the lower catchments of the Karoon, Tigris and Euphrates rivers, the first records of this species outside its native range (Western Atlantic Ocean).These authors also documented the first record of the megabalanine, Megabalanus coccopoma (Darwin, 1854) in the waters of the Persian Gulf and the Gulf of Oman, and stressed the need for a monitoring program to detect newly-arrived exotic species.The subsequent detection of Amphibalanus improvisus on the invasive Hepu mitten crab, E. hepuensis, in the Persian Gulf further supports the case for the monitoring for exotic species.

Table 1 .
Distinguishing features of Amphibalanus species found in the region.CR = carino-rostral.