Sacculina granifera (Boschma, 1973) is a species of rhizocephalan barnacle that commonly parasitises crabs, primarily the commercial sand crab Portunus pelagicus (Linnaeus) in Moreton Bay, Queensland (Sumpton et al.1994). The genus Sacculina contains many species of rhizocephalan parasites, with their crab hosts experiencing a range of physiological and morphological consequences, including but not limited to feminisation and castration (Hartnoll 1967). Sacculina are found across the globe, however S. granifera is currently only known to inhabit certain waters off the eastern and northern coasts of Australia. Most studies pertaining to Sacculina spp. relate to two other species, S. carcini and S.lata, offering information closely related to S. granifera.

As with most sacculinid species, S. granifera draws horror and fascination upon realisation that it is not in fact the crab’s own egg mass. S. granifera is generally oval to rectangular in shape and yellow in colour, and approximately as wide as the abdomen of its crab host. It secretes a chitinous mantle with one aperture for developed nauplius larvae to leave their parent (Day 1935). Rhizocephalan barnacles differ greatly from other barnacles, having two body sections; namely a sac-likeexterna and an inner root system called an interna. Initially, a female rhizocephalan larva enters the host crab with the interna growing from a basal membrane, and the externa growing once the interna has matured. The externa is mainly filled with reproductive organs and can become an egg mass, nurtured by the host crab (Lawler & Shepard 1978). The interna and externa are joined via a peduncle, which attaches to the underside of the crab; this would otherwise be the area on a female crab where developing eggs would be kept (Fig. 1) (Day 1935). Parasitised male crabs may also experience a widening of the abdomen to accommodate the externa of the barnacle, which can grow up to 7cm in width, until the male’s abdomen closely resembles that of a regular female crab (Lawler & Shepard 1978). Infected females, however, generally do not experience any changes in external morphology (Kristensen etal. 2012).

S. granifera, like most other sacculinid species,generally inhabits shallow marine environments but have been known to live in deeper environments (>10m). Rates vary due to seasonality, sex and geographic area, but generally around 10% of mature P. pelagicus are infected by S. granifera (Clarke & Ryan 2004). However, prevalence of the barnacle has been known to reach 29% (Shields & Wood 1993). As infection rates of S.granifera are measured by calculating the percentage of crabs with externae, these rates are obviously underestimations of the true prevalence of the barnacle (Weng 1987). Mature crabs are preferred as hosts as they are more biologically suited to nurture an egg mass, although crabs as small as 7cm long have displayed externae (Weng 1987).

Sacculinid barnacles feed very differently than their shelled relatives in the superorder Thoracica. Instead of filter-feeding from the surrounding water via cirri, sacculinids such as S. granifera have evolved to absorb nutrients from the host crab via the root-like interna. The interna is comprised of a hypha-like network of tubes spreading throughout the entire body of the host (Day 1935). Sacculinid larvae are lecithotrophic, meaning that theonly nutrition they receive is from the yolk originally held in its egg (Kashenko et al. 2002). This means that S. granifera is unlikely to outbreak due to nutrient runoff, as possible resulting phytoplankton blooms due to eutrophication do not provide an increased food source for this species.

Once embryonic nauplius larvae develop eyes, the externa of S. carcini changes from yellow to a dark brown colour (Figs. 1 and 2), signalling that the brood of larvae will be released, usually within three days; a brood can contain males only, females only or a combination of both, usually in equal proportions (Høeg 1984). Following release, nauplii generally metamorphose between four and eight days, with settling possible in the following two to three days (Høeg 1984).

The general life cycle of all sacculinid species consists of two main phases: a free-swimming nauplius larvae with four substages (Fig. 3) and a cyprid stage, followed by the endoparasitic interna stage from which the female externa grows. The nauplius larva of S. carcini has been studied using a scanning electron microscope (SEM) to determine development stage and distinguish features. Each of the four nauplius stages display the characteristic frontal horns of cirripedes and three segmented limbs, a classic feature of small crustaceans (Fig. 4: ml = moulting line, fh = frontal horn, sp = spine, s = seta); each limb has spines called setae arranged in comb rows, with many of the setae exhibiting smaller spikes called setules (Collis & Walker 1994).

S. granifera is indigenous to Australian coastal waters, being found predominantly in Moreton Bay, Queensland, where P. pelagicus is heavily fished both commercially and recreationally. S. granifera has also been found around Mornington Island, in the Gulf of Carpentaria north of Australia, where there is no commercial fishery for P. pelagicus (Fig. 7). Infection rates differ significantly between the two areas, with 6.6% of P. pelagicus displaying barnacle externae in Moreton Bay but only 1.2% of blue swimmer crabs in the Gulf of Carpentaria displayed externae (Weng 1987). It is highly likely that the true distribution of S. granifera is much wider, considering that its host P. pelagicus is an important commercial species across a wide geographical range including the Arabian Gulf (Zainal 2013), but further research is needed to determine if larval dispersal to these areas is possible.

The genus Sacculina is present almost worldwide, occurring predominantly in Australia, Europe and South Africa (Zetlmeisl etal. 2011). The closely related species S. carcini (Thompson) occurs throughout Europe, and is a common parasite on the European green crab Carcinus maenas, one of the most successful invasive species native to Europe and north Africa; C. maenas has been introduced to both North and South America, South Africa and Australia, and hence so has S. carcini (Zetlmeisl etal. 2011). S. lata occurs natively in Japanese seas and was recently discovered in the South China Sea, parasitising the commercial swimming crab Charybdis miles in the Beibu Gulf (Yang et al.2018).

S. granifera belongs to the phylum Arthropoda, the most speciose phylum in the animal kingdom; around 84% of known animal species belong to this phylum. Arthropods are generally distinguished by their chitinous exoskeleton and jointed limbs, as their exoskeleton cannot bend to accommodate movement. Sacculinids have lost the outer hard calcareous shell present in other barnacles; chitin-based structures are generally more flexible than calcite and other calcareous deposits, and hence enable the barnacle to penetrate and spread throughout the body of its crab host more easily.

Taxonomy

Phylum: Arthropoda

Subphylum: Crustacea (Brünnich 1772)

Class: Maxillopoda (Dahl 1956)

Subclass: Thecostraca (Gruvel 1905)

Infraclass: Cirripedia (Burmeister 1834)

Superorder: Rhizocephala (Müller 1862)

Order: Kentrogonida (Delage 1884)

Family: Sacculinidae (Lilljeborg 1860)

Genus: Sacculina (Thompson 1836)

Species: Sacculina granifera (Boschma 1973)

S. granifera, like other barnacle species, is ectothermic; its body temperature is dependent on the temperature of the surrounding water. Previous studies have measured thermal acclimation to short-term temperature change in barnacle cirral activity (Newell 1973), and have found that cirral activity, along with several other rates of movement, is temperature-dependent (Southward 1964). These bodily functions follow a typical temperature curve, that is there is an optimum temperature at which these processes are most efficient. With increasing water temperature due to climate change, these processes may be negatively affected, although further research is needed to determine if Sacculina shares these characteristics with more well-studied species.

As S. granifera visibly presents primarily on blue swimmer crabs, population abundance is usually calculated by infection rates on these crabs, and hence, as P. pelagicus is an important commercial species, minimal research has been conducted into conserving S. granifera; this is because crabs with rhizocephalan infection are either completely unmarketable or worth far less than crabs without infection. This is a similar story for species in Sacculina in general, including species mentioned above. This species and its adaptations are primarily of interest to us commercially as a nuisance pest, and scientifically as a fascinating evolutionary pathway.

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