Matúš Hyžný (Slovakia) and Adiël A Klompmaker (USA)
The term “ghost shrimp” usually refers to decapod crustacean species from the family Callianassidae and Ctenochelidae, although sometimes the term is also used for other crustacean groups, such as caprelloid amphipods or, mostly in aquarium trading, for palaemonid shrimps. Here, we use the first definition. In that respect, ghost shrimps are soft-bodied, fossorial (burrowing) decapods with a tail (or pleon) distinctly longer than the main body (or carapace; Fig. 1). They inhabit a variety of marine environments or environments under marine influence, for example, estuaries, marshes and mangroves. Although most species living today have been described from the intertidal environment, there are numerous species dwelling in deeper waters as well.
Ghost shrimps exhibit a sophisticated behaviour involving digging complex permanent or semi-permanent burrow systems, and they are important bioturbators. Because they live in high densities (in some cases up to 120/m2 of burrow openings are known), they rework huge amounts of substrate and are considered true ecosystem engineers. Bioturbation enhances organic decomposition, nutrient cycling, redistribution of organic material and oxygenation of sediment (similar to earthworms on land). Numerous organisms benefit from these changes, including bivalves, worms and other crustaceans. Additionally, many animal species live directly within the ghost shrimp burrows as their associates.
Not every fossil ghost shrimp is Callianassa
Fossil hunters specialising in decapod crustaceans often identify ghost shrimp specimens as Callianassa or Protocallianassa. However, since the 1980s, researchers on ghost shrimps living today have attempted to divide the genus Callianassa into several independent genera. Now, there are some fifty distinct ghost shrimp genera recognised, including several known exclusively from the fossil record.
A broadly defined concept of Callianassa has been used many times in the past for fossils: any ghost shrimp with a mainstream claw morphology has been attributed to Callianassa and, as a result, 190 species have been described under the collective taxon “Callianassa”. No attention has been paid to many of them since the first description. Similarly, many species have also been ascribed to Protocallianassa; and this genus has been used for almost any callianassid remain from the Cretaceous. Callianassa and Protocallianassa, so well-established in the palaeontological literature, appear to be “waste-basket taxa”, that is, they do not represent natural biological units. Instead, they represent a mixture of distinct genera. Since recognising this problem, only 4 (out of 56) newly erected fossil ghost shrimp species have been attributed to Callianassa by palaeontologists since 2000.
Ghost shrimps in the fossil record
While true crabs (Brachyura) are one of the best-preserved crustacean groups in the fossil record, ghost shrimps are one of the most ubiquitous. Their remains are present in most assemblages of Late Cretaceous and Cenozoic decapod crustaceans described so far. All Jurassic species previously referred to Callianassa have turned out to be representatives of the family Axiidae. No undoubted ghost shrimp older than the Hauterivian (about 130Ma) is known to date. Since the Early Cretaceous, ghost shrimps have become common macrofaunal elements in many decapod fossil assemblages. Based on recent research, as many as 252 valid fossil ghost shrimp species are known and 25 (10%) of them have been described since 2010. We are truly living in the golden age of the fossil ghost shrimp research.
Preservation of ghost shrimp fossils
Only the hardened parts of ghost shrimps are usually preserved, due to the delicate nature of most of the shell (or cuticle). Heavily calcified claws are preserved most frequently, although other parts are sometimes preserved as well. Three main types of preservation in terms of completeness of the material can be observed for fossil ghost shrimps (Fig. 2) as discussed below.
- (Near) complete body fossil: well-preserved decapod crustacean. While some parts may be missing, the majority of all three main parts of the shrimp should be present (that is, carapace, legs and pleon). Whole-body fossils of ghost shrimps are rare – of the 252 valid fossil ghost shrimp species, only 19 species (7.5%) were originally described from whole-body fossils. They usually represent moults with the first pair of legs (chelipeds) positioned anteriorly to the rest of the body. The carapace is flipped over, whereas the pleon is bent inward, so that the end part of the tail (or telson) points towards the head of the animal.
- Disassociation unit: a natural aggregation of exoskeleton elements commonly preserved together. As ghost shrimps decompose, they disintegrate into disassociation units comprised of the more heavily calcified parts of the exoskeleton. Disassociated chelipeds are more common than disassociated pleonal units: 92 species (36.5% of all valid species) were described using the first pair of legs including the claw consisting of at least three elements, usually preserved as a disassociation unit.
- Isolated elements: single part of the exoskeleton found without any associated parts from the same specimen. If the cheliped disassociation unit disintegrates further, only often fragmentary, isolated cheliped elements remain. This mode of preservation constitutes the most abundant portion of the ghost shrimp fossil record: 160 species (63.5%) were originally described based on isolated elements of the claws (dactylus and/or propodus).
Preservation in burrows
The fossorial behaviour of the ghost shrimps is often preserved in the fossil record as trace fossils representing burrows. Several trace fossil genera (or ichnogenera) have been attributed to decapod crustaceans by direct comparison with extant ghost shrimp burrows, that is, Ophiomorpha, Thalassinoides and Spongeliomorpha. Sometimes, even the producer of these burrows has been found inside. The preservation of a whole-body ghost shrimp found within a burrow structure (Fig. 3) can be explained by death or moulting within a burrow followed by rapid burial and fossilisation.
Identification of fossil ghost shrimps
The fossil record of ghost shrimps is relatively rich in comparison with other decapod groups. However, the interpretation of their fossils can be challenging, mainly because the assignment of ghost shrimps to the genus level is often hindered by their incomplete preservation. Many extant genera are differentiated based on weakly calcified characters with low or no fossilisation potential, so these taxa will remain unrecognised in the fossil record if not re-diagnosed to include hard-part morphology. Finding characters present on well-calcified chelipeds that are consistent throughout the genera is essential to better classify fossil remains.
Variation within and across species, heterochely (see box: Heterochely) and sexual dimorphism, as well as ontogenetic changes (that is, changes occurring from fertilisation through to the mature form) are all known to occur in this group. These factors need to be taken into account while identifying isolated ghost shrimp fossils, which makes this group exciting to work with at the same time.
Heterochely is a condition in decapods where the two claws of an individual differ in size, shape and often function, which usually occurs in both sexes of a species. In many decapod taxa, heterochely becomes more apparent in larger specimens and it is generally more obvious in males. Ghost shrimps are usually strongly heterochelous as only a few taxa exhibit equally-sized chelipeds. Minor chelipeds are often distinctly different from major ones other than size (Fig. 4). This has sometimes led erroneously to the recognition of two separate species in the fossil record, especially when dealing with isolated cheliped elements. There is a complete lack of preference of handedness in ghost shrimps, which means that populations consist of a nearly equal number of left-handed and right-handed individuals.
The chelipeds are sexually dimorphic in some ghost shrimp species because the major cheliped becomes larger and more massive in mature males. Sexually dimorphic chelipeds, accompanied by growth whereby one dimension grows faster than another increases the differences between male and female chelae, have been demonstrated convincingly for several ghost shrimp genera. Sexual dimorphs can express not only different growth rates of chelipeds, but also different morphologies of the major chela (Fig. 5). Differences in the sexual morphs can even lead to the incorrect recognition of two separate taxa.
What the future holds
Fossil ghost shrimps have become an active field of research in the last decade. We have achieved numerous new insights into the life of these fascinating animals, not only in terms of understanding their ecology and behaviour, but also in evaluing their taxonomic richness in the fossil record. We are now much better at interpreting isolated remains of ghost shrimps. One of the main goals of current research is to reconstruct the evolution of burrowing behaviour of this particular group of decapod crustaceans. One key question is how ghost shrimps became such successful ecosystem engineers. We do believe that the next ten years will bring an answer to this question.
About the authors
Matúš Hyžný is currently a researcher at Comenius University, Bratislava (Slovakia). Much of the presented research was carried out when he was a postdoctoral researcher at the Natural History Museum in Vienna (Austria).
Adiël Klompmaker is currently a postdoctoral scholar at the University of California, Berkeley (USA).
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