Paracerceis sculpta is a small marine isopod of the Sphaeromatidae family which has become a formidable global invader. Tolerant of a wide range of environmental conditions, this species has established populations in ports and surrounds worldwide. P. sculpta has been extensively studied as a model organism for male sexual polymorphism and alternative reproductive strategies. This webpage seeks to consolidate current information on the species and will describe parental care behaviours observed in the laboratory.

Specimens collected for study were identified with the expert assistance of Dr Niel Bruce, Senior Curator of tropical marine biodiversity at the Museum of Tropical Queensland. Identification to family level was achieved using a key developed and provided by Bruce (n.d.). 

I would like to express my gratitude to Dr Niel Bruce of the Queensland Museum for his kindness, swift replies and expert assistance in the identification of this isopod specimen. 

Colouring (and therefore initial physical appearance) is extremely variable among isopods, with P. sculpta being no exception. During profiling, two specimens were collected: an adult female and an unsexed juvenile. The adult individual collected displayed a black cephalon, a broad white stripe over the pereon with dark sides, and a mixed-colour pleotelson, with the upper portion dark and the lower section white (Figure 1). This specimen was measured at 4.1mm long, well within the 1-10mm size range for the species. The juvenile specimen was devoid of colouration, possessed six pairs of pereopods and was approximately 1mm long (Figure 5). The body was somewhat flattened dorso-ventrally, though it retains a rounded dorsal surface. Three short ridges on the pleotelson were present, characteristic of the female of this species (Katsanevakis et al.,2014) (Figure 4). Compound eyes were well developed and situated directly on the sides of the cephalon. Seven pairs of pereopods approximately equal in length were present. Antennae were approximately one third of the length of the body, with antennules slightly shorter. The apex of the pleotelson displays a concave boundary. Uropods were flattened and similar in length, with small setae along the border. Pleopods did not extend the full length of the pleotelson.

Mouth parts (not observed on the adult specimen here) are common to all individuals within the species with the exception of ovigerous females and are comprised of mandibles, maxillipeds and two pairs of maxillae (Harrison & Holdich, 1992).

External female anatomy was in line with the stage five descriptions of Shuster (1991) in which females have undergone their reproductive moult and possess metamorphosed (non-functional) mouth parts fused to the cephalon, some setae on segment margins and a brood pouch.

The species displays strong sexual dimorphism, which will be explored further in the following subsections. 


Female characteristics

Non-ovigerous females

Katsanevakis et al. (2014) outlines the following female character traits:

1. Pleotelson displays three short longitudinal ridges (Figure 3).

2. Uropods are flattened, similar in length, and do not reach the apex of the pleotelson (Figure 2).

3. Apex of pleotelson displays a concave boundary (Figure 2). 

Ovigerous females

Shuster (1991) characterises ovigerous females as similar in overall body conformation to non-ovigerous females, with the notable exceptions of:

1. Setae along segment margins (visible in Figure 1).

2. Metamorphosed (non-functional) mouthparts, fused to the cephalon.

3. Brood pouch present.

4. Loss or degradation of cuticular colouration.

 Male characteristics
              
  Alpha 
Alpha males are the most different to other members of this species. They are the largest of the male morphs, and larger than females. Katsanevakis et al. (2014) outlines the following alpha male character traits:
1. Modified pleotelsonic apex with a deep notch in which the margin is toothed (Figure     3).
2. Three long, hairy ridges protruding from the pleotelson, with the central ridge larger than the outside ridges (Figure 3, modified pleotelson).
3. Heavily modified exopod: very long, pointed, curved (Figure 3).

                Beta
Beta males are similar in size and appearance to females, though possess male reproductive organs (Munguia and Shuster, 2013; Shuster, 1992) (Figure 3).

                Gamma
Gamma males are similar in appearance to females, though much smaller and possess male reproductive organs (Munguia and Shuster, 2013; Shuster, 1992) (Figure 3).

P. sculpta, native to the Gulf of California and Mexico, is typically found in intertidal waters or relatively shallow subtidal waters (Espinosa-Pérez and Hendrickx, 2001). It occupies a shallow-water habitats including rocky shores, algae (upon which it feeds) and calcareous intertidal sponges (where it breeds), as well as occurring on sandy substrates in deeper water (Espinosa-Pérez and Hendrickx, 2001). Individuals (particularly females as they search for a suitable spongocoel) face a risk of predation from fishes in migrating from their algal feeding grounds to the intertidal sponges in which they breed (Shuster, 1990).

Like other Peracarid isopods, P. sculpta exhibits a limited natural dispersal capability (Hewittand Campbell, 2001). An association occurs between P. sculpta and the biofouling bryozoan Amathia verticillata (Dailianis et al., 2016) and increased likelihood of P. sculpta occurring in non-native waters where A. veticillatais present indicates A. verticillata may have a role in facilitating the biofouling-associated spread of P. sculpta on international vessels. As yet, no evidence of negative effects from non-native populations of P. sculpta have been found. 

Life cycle

P. sculpta follows a life cycle typical of all Peracarid crustaceans, in which embryos undergo direct development (Brusca, 1997). Priorto mating, females undergo a reproductive moult which renders them unable to feed and initiates the development of the ventral brood pouch. Embryos develop from eggs deposited into the inseminated female's brood pouch (Shuster, 1991). Embryos take between two and nine weeks to develop into a fully-formed juveniles (mancae) ready to disperse from the brood pouch (Shuster, 1991).Females always die within 2 weeks of mancae dispersal (Shuster, 1991).

Reproductive behaviour

Shuster (1987, 1990, 1992) and Shuster and Wade (1991a, 1991b) have extensively studied the reproductive behaviours of the three male morphs of P.sculpta among native population dynamics. The intricacies of the mate selection process are slightly modified amongst non-native populations, which have been found to be comprised only of females and alpha male types (Marchini, Costa, Ferrario and Micael, 2017) and lack the additional (non alpha-alpha) male-male competitive interactions of native populations.

Reproductive activities of P. sculpta typically take place in sponges of the intertidal zone, leaving the algae they feed on to enter spongocoels (Shuster, 1992). All three male morphs within a community employ different reproductive strategies. Alpha males, the largest and most common of the male morphs, adorned with elongated exopods and a modified pleotelson, inhabit and defend spongocoels against other male intruders (Shuster, 1992). Beta males, the least common of the male morphs, are morphologically similar to females and imitate the behaviour of sexually receptive females in order to gain access to an active spongocoel community (Shuster, 1992). Gamma males are the smallest, though otherwise similar in body conformation to females, and employ 'sneak' tactics using their speed and small size to evade defensive alpha males (Shuster, 1992). Despite employing vastly different approaches to aquiring mating partners, all three morphs are capable of mating successfully, though the relative density of particular male morphs and females within a spongocoel aggregation affects the fertilisation success of each male (Shuster& Wade, 1991a), thus perpetuating the unequal proportions of each male morph within the species.

Male interactions typically occur in competition with the dominant alpha male of a particular spongocoel aggregation. Alpha males will attempt to invade and take over another alpha's spongoceol and mate with the sexually receptive females within (Shuster, 1992). Intruding alpha males, while consistently more aggressive, are most often unsuccessful in takeover attempts, though size confers a significant advantage (Shuster, 1992). Alpha males resist intrusion of the spongocoel by gamma males in a similar way, though the gamma male often succeeds in entering after multiple invasion attempts due to its small size and considerable speed (Shuster, 1992). Interactions between alpha and beta males follow patterns typical of a male-female interaction in which the beta male initiates tactile stimulation of the alpha in the same manner as a female (Shuster, 1992).

Females show limited selectivity when it comes to finding a mate: while they prefer larger males overall, they show no signs of discrimination between males within a similar age range (one month) and body length (within 10%), and will mate with any male available (Shuster, 1990). This type of relatively uninformed partnering is characteristic of semelparous species, as they have a limited period of time in which to find a mate, and a lack of prior experience in choosing a suitable breeding partner. Sexually receptive females seek out males inhabiting spongocoels in order to initiate courtship. They exhibit a preference for spongocoels already containing gravid females, as do intruding alpha males (Shuster, 1990). The courtship process is typically short, with females initiating oral contact, and the male responding by shaking her vigorously (Shuster, 1990). Soon after, mating occurs.

Dr Stephen Shuster is recognised as an authority on the mating behaviours of P.sculpta, and readers seeking more information are directed towards his many publications.

 Observed juvenile care

An apparent degree of juvenile care was observed in the collection of a female specimen with offspring. The female tucked the juvenile underneath her body, occasionally holding it in place with 2-4 pereopods. Upon separation, the female apparently tried to re-capture the juvenile by rolling onto her back nearby and repeatedly fanning her legs inwards. When the juvenile moved to a different location, the female followed until the pair were reunited. This reflects a level of parental care until the young are developed enough to permanently disperse from the brood pouch. As some browsers block embedding within this webpage, please visit the following link to view a video of the gravid female with a near-fully formed manca.

https://www.youtube.com/watch?v=EBtISBlDf0Q

Uropods

Uropods, as in all Peracarid crustaceans, function as swimming appendages in P. sculpta. They are comprised of an endopod and exopod, and typically possess setae on the borders. However, in this species, the alpha male form possesses a highly modified uropod in which the exopod is greatly elongated (Katsanevakis et al., 2014). These uropods are used to grapple with other males in competition for female breeding partners (Shuster and Arnold, 2007).     
            

Changes in female anatomy with the reproductive moult

Perhaps the most interesting anatomical aspect of P. sculpta is the drastic changes the female undergoes during the reproductive moult. This moult readies the female for reproduction, but also restricts her mobility and eliminates her ability to feed (Shuster, 1991). For this reason, P. sculpta is a semelparous species - females are only able to reproduce once before death.

Externally, pre-moult females possess healthy, lustrous cuticles, functional mouthparts and a slightly convex ventral cuticle (Shuster, 1991). The genital pore is not formed in pre-moult females, though a depression in the cuticle is present, indicating the post-moult position of the pore (Shuster, 1991). Internally, the hepatopancreas and ovaries are conspicuous from a ventral view in pre-moult females (Shuster, 1991).

In post-moult females, the cuticle is dulled and progresses towards transparent or white as the female approaches death (Shuster, 1991). Filled brood pouches occupy the majority of the space within the ventral body cavity and push other organs, including the hepatopancreas, dorsally or anteriorly into the cephalon (Shuster, 1991). Mouthparts are rendered useless following the anterior moult, in which they are fused to the cephalon (Shuster, 1991). Though vestigial appendages remain, they are devoid of pre-moult setae and lack molar and incisor processes (Shuster, 1991). Because of the degree of anatomical change, all post-moult females will die within two weeks of mancae release (Shuster, 1991). 

P. sculpta is native to the northeastern Pacific region, concentrated particularly in the intertidal waters of Southern California through to Mexico (Espinosa-Pérez and Hendrickx, 2001). This isopod has proven to be a hardy species and a proficient global invader (Marchini, Costa, Ferrario & Micael, 2017). It is typically found in tropical or temperate waters and is able to tolerate a wide range of salinities, depths (shallow to 200m) and silt loads (Espinosa-Pérez and Hendrickx, 2001; Katsanevakis et al., 2014; Hewitt and Campbell, 2001).

Introduced populations are typically centred around global ports, suggesting introduction via biofouling of vessels (Marchini, Costa, Ferrario and Micael, 2017; Espinosa-Pérez and Hendrickx, 2001; Rodriguez, Drake and Arias, 1992; Hewitt and Campbell, 2001). Though there has been no widespread survey of P. sculpta's global distribution, specimens have been collected from Australia (Hewitt and Campbell, 2001), Japan (Ariyama and Otani, 2004), Hong Kong and Southern China (Bruce, 1990), Brazil (Pires, 1981), Hawaii (Miller, 1968), the Atlantic coast of Europe (Spain, Portugal) (Rodriguez, Drake and Arias, 1992; Marchini, Costa, Ferrario and Micael, 2017) and the Mediterranean Sea (Dailianis et al., 2016).

In Australia, the first identification of P. sculpta occurred in Townsville QLD (Hewitt and Campbell, 2001). Since then, populations have been established in 13 locations nation-wide through domestic and international translocation(Hewitt and Campbell, 2001).

An interesting note on P. sculpta's distribution is the absence of two of three male morphs in non-native populations, with beta and gamma males only present in populations within the species' native distribution (Marchini, Costa, Ferrario and Micael, 2017). 

The currently accepted taxonomy of P. sculpta according to Schotte (2008) is as follows:

Kingdom ANIMALIA

Phylum   ARTHROPODA

Subphylum CRUSTACEA

Class MALACOSTRACA

Subclass EUMALACOSTRACA

Superorder PERACARIDA

Order ISOPODA

Suborder SPHAEROMATIDEA

Superfamily SPHAEROMATOIDEA

Family SPHAEROMATIDAE

Genus Paracerceis

Species Paracerceis sculpta

P. sculpta was originally placed within the genus Dynamene (Holmes, 1904) until being redefined and placed within the genus Paracerceis upon its designation soon after. Paracerceis angra (initially Sergiella angra) (Pires, 1980), was identified as a misidentification of P.sculta and has since been accepted as a junior synonym (Pires, 1981). P. sculpta is one of 13 independently accepted species within its genus.

Isopods are a diverse group, with members inhabiting marine (most numerous and diverse), fresh water and terrestrial environments (Brusca,1997). Phylogenetic analyses suggest that members of Isopoda date to at least the Carboniferous Period (Brusca, 1997). 

P. sculpta is a hardy species with an expanding global range and is not considered threatened. It would be unwise, however, to enact no conservation or monitoring programs in its native habitats. Two of three male morphs are only present in native populations, suggesting a greater diversity within these populations which we should aspire to preserve. 

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