Who would like to carry a parasite? I bet not many people would like to have one or more. They are nevertheless very common in humans and in other organisms, and can affect entire food webs including keystone species. They tend to be small compared to the host and the vast majority of them are soft-bodied. Despite their small size and soft appearance, they can affect the host substantially, for example, leading to a reduced growth rate and less offspring.
Much of the same holds true for crustaceans – they are affected by parasites and can act as parasites themselves. For example, parasitic crustaceans are found among the isopods and copepods. Given the widespread occurrence of parasitism in and by crustaceans today, a fossil record of such parasitism may be expected.
Swellings in fossil crabs and squat lobsters
So what does the fossil record look like? I have been fortunate to have worked on this under-studied field of research. During my PhD research, I found various swellings in fossil crabs and squat lobsters (decapods from the superfamily Galatheoidea) during and after field work in northern Spain in reef carbonates from the mid-Cretaceous (upper Albian). They appeared to occur regularly in the back part of the carapaces of these crustaceans.
This swelling is almost certainly a trace fossil of a parasite. It very much resembles swellings made by modern isopods of the Bopyridae family. They enter the decapods as larvae, transform to an adult isopod after attachment on the inside of the shell in the gill region from which they draw blood, and affect decapod growth and rate of reproduction negatively. The first larva becomes a female, whereas a male, much smaller specimen may develop later (Fig. 1). The shell of the crab or lobster is expanded by the isopod (Fig. 2), especially after moulting. For that reason, many researchers have called fossil decapods with such a bulge ‘bopyrid’ or ‘bopyriform swellings’. However, given that some other isopods can also cause similar swellings in these crustaceans and we are dealing with traces as early as the Jurassic, it is more appropriate to call them isopod swellings or, even better, use its trace fossil name, Kanthyloma crusta.
Unfortunately, soft-bodied isopods do not preserve very well so that, so far, no such isopod has been found inside a decapod corpse with a swelling. However, larvae attributed to Bopyroidea or Cryptoniscoidea (both isopod groups that parasitize decapods) have been found recently in Miocene amber.
Trouble for Spanish decapods
Even though the shell or cuticle was dissolved for the Spanish crustaceans, no isopod fossil was found in the internal mould either. Not all species were equally affected by parasitism after careful study of specimens that were complete enough to be able to observe whether or not the specimen showed a swelling. For example, 12% of the squat lobster Eomunidopsis navarrensis showed a swelling, whereas another (but less abundant species, the crab Goniodromites laevis) was infected only at 1% (Fig. 3). More common species tend to show a higher percentage of Kanthyloma crusta, also when statistics are used. Although this novel result needs to be tested for more assemblages, it may mean that parasitic isopods target abundant species.
Infestation trends through time
The very interesting results from one outcrop add to an already existing list of infested fossil Decapoda (Fig. 4). After updating and expanding this list, I investigated trends through time from the Jurassic to the Holocene, because infestation rates through time were unknown.
A low number of non-squat lobsters and shrimps were found with a swelling. These lobsters may have genuinely not been infested heavily as their carapaces are often preserved, whereas the carapaces of fossil shrimps are rarely preserved, so swellings are not found easily in this group. Conversely, squat lobster and crab species do show frequent swellings. Plotting the number of species with swellings for each epoch shows peak infestation during the Late Jurassic for these two groups and, as a result, also for all Decapoda combined (Fig. 5).
The problem here is that the Late Jurassic is known to harbour a lot of decapod species, mainly found in reef deposits, compared to other Mesozoic epochs. The peak infestation during the Late Jurassic may therefore simply be a product of a high species diversity. However, peak infestation remains present when we look at the percentage of all species that is infested in each Mesozoic epoch (Fig. 5, inset). Kanthyloma crusta is rarely found in the late part of the Cretaceous and in the Cenozoic, despite high diversities during parts of the Cenozoic and unsuccessful efforts by multiple people to find many swellings from these periods.
The Late Jurassic peak
So what caused the peak and subsequent decline around the Late Jurassic? This pattern may be either caused by biases inherent to the fossil record or it might be a true biological signal. As mentioned above, a bias towards preferential collecting of specimens with Kanthyloma crusta is unlikely. A preservational bias is unlikely as well, because decapods from the Late Jurassic are not better or less preserved than those in other periods and those from the same deposits: carapaces are often broken hampering the recognition of swellings. Instead, the pattern may be a biological one.
We can speculate that the initial rise could be caused by the fact that decapods were not used to these parasitic isopods and were unable to fend them off. Consequently, the isopods increased in abundance along with the decapods in the Late Jurassic, and affected more and more species.
The decline in the percentage of decapod species infected can be explained by multiple reasons. The two most likely are related to adaptation and the demise of infestation-prone groups. The squat lobsters and certain crab families, such as the Goniodromitidae, declined dramatically around the Jurassic/Cretaceous boundary. The larvae of the parasites must have had a harder time finding different taxa so that fewer taxa were affected. An alternative is that decapods developed habits to either keep the larvae of isopods outside their gills or developed more effective ways to remove the parasite once infected. Research on extant representatives may help to elucidate this.
This type of parasitism is really well-known compared to other types of parasitism involving crustaceans in deep time, as shown by a recent review article ([REF?]). For almost all epochs and many stages, swellings are known. However, new research on Kanthyloma crusta should be done to continue to test patterns and to test host specificity. At the very least, such evidence of parasitism can be reported alongside systematic descriptions of new or known taxa.
More affected crustaceans
Other examples of palaeoparasitism in or by crustaceans include barnacles infesting crabs leading to feminisation of males, other barnacles negatively affecting corals and echinoids, crescent-shaped traces (domiciles) of crabs from the family Cryptochiridae that probably negatively affected coral growth, and copepods infesting echinoids and crinoids (Fig. 6). All this evidence is based on traces only, but sometimes the parasite bodies themselves are preserved. Two examples are known. Parasitic copepods were found in the skull of a Cretaceous fish. Secondly, the tiny pentastomids or tongue worms, considered to represent crustaceans by part of the community and known to be parasitic today, have been found as isolated fossils as early as the Late Cambrian. All these examples are known from only one or very few epochs so far and also require more research.
The book Fossil Crustaceans, published at the end of last year, is the most up to date work on parasites in the fossil record. This work shows that the field of palaeoparasitology is an active field of research. What can be found in your personal collection or in the collection of a museum nearby?
About the author
Adiël Klompmaker currently is a postdoctoral scholar at the University of California, Berkeley. Most of the presented research was carried out when he was a post doctorate at the Florida Museum of Natural History at the University of Florida. Specimens were mostly collected when he was a PhD student at Kent State University (Ohio, USA).
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