Overview
Caprella mutica, commonly known as the Japanese skeleton shrimp, is a species of skeleton shrimp. They are relatively large caprellids, reaching a maximum length of . They are sexually dimorphic, with the males usually being much larger than the females. They are characterized by their "hairy" first and second thoracic segments and the rows of spines on their bodies. Body color ranges from green to red to blue, depending on the environment. They are omnivorous highly adaptable opportunistic feeders. In turn, they provide a valuable food source for fish, crabs, and other larger predators. They are usually found in dense colonies attached to submerged man-made structures, floating seaweed, and other organisms. C. mutica are native to shallow protected bodies of water in the Sea of Japan.
In as little as 40 years, they have become an invasive species in the North Atlantic, North Pacific, and along the coasts of New Zealand. They are believed to have been accidentally introduced to these areas through the global maritime traffic and aquaculture. Outside of their native range, C. mutica are often exclusively synanthropic, being found in large numbers in and around areas of human activity. Their ecological and economic impact as an invasive species is unknown, but they pose a serious threat to native populations of skeleton shrimp in the affected areas.
Description
Like all caprellid amphipods, Caprella mutica are characterized by slender bodies and elongated appendages. Their skeletal appearance gives rise to the common names of "skeleton shrimp" or "ghost shrimp", and, coupled with their distinctive upright feeding posture, give them a striking resemblance to stick insects and "starved praying mantises". C. mutica vary in coloration from translucent pale green, brown, cream, orange, deep red, purple, and even turquoise, depending on the substrate they are found in. The brood pouches of the females are speckled with red spots. A relatively large amphipod, C. mutica are sexually dimorphic with males considerably larger than females. Males average at a length of , Females, on the other hand, average at only long. The body can be divided into three parts – the cephalon (head), the pereon (thorax), and the abdomen.
The second pereonite also has two to three pairs of spines on the back, with an additional two pairs at the sides near the base of the limbs. The third pereonite has seven pairs of spines at the back while the fourth pereonite has eight pairs. Both have three to seven pairs of spines near the base of the gills. The fifth pereonite has five pairs of back spines and a pair of spines at the sides. The sixth and seventh pereonites each have two pairs of back spines, situated at their centers and near the posterior. Like other crustaceans, C. mutica possess two pairs of antennae, with the first (outer) pair more than half the total length of the body. Despite the name, it remains unclear if the poison spine is indeed venomous, though they are perfectly capable of inflicting potentially lethal injuries on small organisms.
Recent studies have associated the spines with pores that lead to possible toxin-producing glands. Their dactyli are powerful and curved into a scimitar-like shape. The fifth to seventh pereopods function as clasping appendages. They all have propodi with two spines on their inside margins. The seventh pair of pereopods are the longest of the three pairs, followed by the sixth pereopod pair and the fifth pereopod pair. C. mutica closely resemble Caprella acanthogaster, also a native of East Asian waters. It may be difficult to distinguish the two species, particularly since Caprella mutica can exhibit considerable morphological variations among males. C. mutica can only be reliably differentiated by their setose first and second pereonites (smooth in C. acanthogaster), as well as the elongated oval shape of their gills (linear in C. acanthogaster).
Taxonomy and nomenclature
Caprella mutica were first described in 1935 by A. Schurin from specimens collected from the Peter the Great Gulf in the Sea of Japan. It belongs to the genus Caprella in the subfamily Caprellinae of the family Caprellidae, a group of highly specialized amphipods commonly known as skeleton shrimp. Caprellids are classified under the superfamily Caprelloidea of the infraorder Caprellida. C. mutica are known as koshitoge-warekara ("spine-waist skeleton shrimp") in Japanese. Caprella acanthogaster humboldtiensis, another invalid name of the species, was first applied to misidentified specimens of C. mutica recovered from Humboldt Bay, California by Donald M. Martin in 1977. Some specimens collected from the Firth of Clyde, Scotland in 1999 were also initially misidentified as Caprella tuberculata, but have since been determined to be introduced C. mutica.
Ecology and biology
Caprella mutica inhabit shallow protected marine bodies of water. However, in their native habitats, it has been observed that they can survive salinities as low as 11 psu. They are also sensitive to exposure to air, and will die within an hour if taken out of the water. are incubated for about 5 days at in the female's brood pouch. Upon hatching, they reach sexual maturity in about 21 to 46 days. Their average lifespan in laboratory conditions is 68.8 days for males and 82 days for females.
Habitat
In their native habitat, Caprella mutica are found in the infralittoral (or neritic) and littoral zones of sheltered bodies of water to a depth of about . C. mutica are poor swimmers and move around predominantly in an undulating inchworm-like fashion, using their posterior pereopods and gnathopods. In both their native and introduced ranges, C. mutica are also synanthropic, being found abundantly in fouling communities in artificial structures like submerged ropes, fishing nets, pilings, docks, buoys, aquaculture equipment, oil rig platforms, ship hulls, and even offshore wind farms. In their introduced ranges (particularly in Europe), they are primarily and even exclusively found inhabiting artificial structures. Populations reach peak numbers during the late summer (August to September) before experiencing a sharp decline in the winter months.
Diet and predators
Caprella mutica are omnivorous highly adaptable opportunistic feeders. Introduced populations of C. mutica have become a major part of the diets of native wild and farmed fish.
Reproduction and life history
Wild populations of Caprella mutica show a higher number of females than males. This may be related to the fact that females are aggressively defended by males from competing males, resulting in high male mortality. A brood pouch of a female can contain 3 to 363 eggs, averaging at 74 eggs. Larger females tend to produce more eggs. The eggs are incubated inside the brood pouch for 30 to 40 days before hatching. Like all amphipods, caprellids lack a planktonic larval stage and the hatchlings resemble miniature adults. The juveniles may cling to their mothers upon hatching and the females continue to protect their offspring that remain close. Hatchlings measure around and grow to an average of per instar.
Distribution and invasive ecology
Caprella mutica are native to the subarctic regions of the Sea of Japan in northwestern Asia. They were first discovered in the Peter the Great Gulf in the federal subject of Russia, Primorsky Krai. They were redescribed by the Japanese marine biologist Ishitaro Arimoto in 1976 who noted that they were also present in the island of Hokkaido and surrounding regions. In a span of only 40 years, they have spread into other parts of the world through multiple accidental introductions (both primary and "stepping stone" secondary introductions) from the hulls or ballast water of international maritime traffic, aquaculture equipment, and shipments of the Pacific oyster (Crassostrea gigas). Europe and eastern North America are also the possible sources for the New Zealand C. mutica population.
North America
The first specimens of C. mutica outside of its native range was recovered from Humboldt Bay, California by Donald M. Martin in 1973. Martin misidentified them as a subspecies of C. acanthogaster. He named them Caprella acanthogaster humboldtiensis. Additional specimens (also treated as C. acanthogaster or C. acanthogaster humboldtiensis) were recovered between 1976 and 1978 from the Oakland Estuary, Elkhorn Slough, and San Francisco Bay. It wasn't until 1981, when the specimens were correctly identified as C. mutica by Dan C. Marelli. Along with additional specimens discovered in 1983 in Coos Bay, Oregon, these populations are believed to have been introduced to the area as a result of the importation of oyster spat of the Pacific oyster (Crassostrea gigas) from Japan for oyster farming.
Oysters are usually transported with algae as a packing material, particularly Sargassum muticum in which C. mutica are associated with. C. mutica were also discovered in Ketchikan, Sitka, Juneau, Cordova, Kodiak, Kachemak Bay, Prince William Sound, and Unalaska in Alaska between 2000 and 2003. This was the first instance of a non-native marine species being found in the Aleutian Islands. In 2009, they were discovered to have spread into British Columbia, Canada. This indicates that C. mutica have completely expanded up the entire west coast of North America. In 2003, surveys by the Massachusetts Institute of Technology (MIT) Sea Grant along the Atlantic coast of the United States revealed multiple established populations in seaports along the coastlines of Connecticut to Maine.
In the same year, C. mutica were also reported in Passamaquoddy Bay and Chaleur Bay of New Brunswick and Quebec, Canada.
Europe
C. mutica populations in Europe were first found in the Netherlands in 1995. During a species inventory, several specimens of an unknown caprellid were recovered by Platvoet et al. from artificial structures in and around the Neeltje-Jans and the Eastern Scheldt storm surge barrier in Burghsluis, Zeeland. As with the case of the first discovery of C. mutica in North America, Platvoet et al. initially misidentified them as a new species. Remarking upon the resemblance of the caprellids to C. acanthogaster, they named it Caprella macho. They exist in extremely dense populations and are all associated with areas of high human activity. They are believed to have been introduced through shipping and aquaculture equipment from the United States and Asia.
As of 2011, there have been no recorded sightings of C. mutica around the Iberian Peninsula, the Baltic Sea, or the Mediterranean Sea.
New Zealand
Caprella mutica were first detected in New Zealand in the port of Timaru, South Island in 2002. This was the first incident of C. mutica being reported in the southern hemisphere. Since then, more well-established populations of C. mutica have been found in Port Lyttelton in 2006, and in the Marlborough Sounds and Wellington Harbour in 2007. Additional specimens were also recovered from the hulls of vessels in other ports, though they did not seem to have established colonies in the ports themselves. Genetic studies of the New Zealand populations suggests a possibility that these were secondarily introduced from non-native populations of C. mutica in the Atlantic through ballast water in the sea chests of international shipping.
Impact
The direct environmental and economic impacts of introduced C. mutica populations remain unknown. In Europe, wild and farmed fish like the common dab (Limanda limanda), European perch (Perca fluviatilis), and the Atlantic salmon (Salmo salar), consume large amounts of non-native C. mutica. C. mutica fouling populations may also incur minor economic effects through the cost of their removal from submerged aquaculture equipment and ship hulls.
Control
There are no known effective control measures for invasive Caprella mutica populations as of 2012. It has been suggested that the seasonal population fluctuations may be taken advantage of. Eradication efforts done during the winter months when C. mutica populations are dormant and at their lowest numbers, are potentially more effective in preventing their recovery during the summer months. Because of the great difficulty in detecting and removing them, however, control methods will likely focus on preserving native species populations rather than the eradication of established C. mutica.
See also
*List of invasive species *List of the world's 100 worst invasive species