Filtering out parasites: sand crabs (Lepidopa benedicti) are infected by more parasites than sympatric mole crabs (Emerita benedicti)

Abstract

Two digging decapod crustaceans, the sand crab species Lepidopa benedicti and the mole crab species Emerita benedicti, both live in the swash zone of fine sand beaches. They were examined for two parasites that infect decapod crustaceans in the region, an unidentified nematode previously shown to infect L. benedicti, and cestode tapeworm larvae, Polypocephalus sp., previously shown to infect shrimp (Litopenaeus setiferus). Lepidopa benedicti were almost always infected with both parasite species, while E. benedicti were rarely infected with either parasite species. This difference in infection pattern suggests that tapeworms are ingested during sediment feeding in L. benedicti, which E. benedicti avoid by filter feeding. Larger L. benedicti had more Polypocephalus sp. larvae. The thoracic ganglia, which make up the largest proportion of neural tissue, contained the largest numbers of Polypocephalus sp. larvae. Intensity of Polypocephalus sp. infection was not correlated with how long L. benedicti remained above sand in behavioural tests, suggesting that Polypocephalus sp. do not manipulate the sand crabs in a way that facilitates trophic transmission of the parasite. Litopenaeus setiferus may be a primary host for Polypocephalus sp., and L. benedict may be a secondary, auxiliary host.

Keywords: Cestode; Crustacean; Digging; Hippoidea; Nematode; Parasite; Parasite manipulation of behavior.

Figure 1. Digging crab species.

(A) Lepidopa benedicti. (B) Emerita benedicti.

Figure 2. Hypothesized life cycle of Polypocephalus sp.

Larval stages of cestode tapeworms in the genus Polypocephalus infect crustaceans and other invertebrates. These intermediate hosts are presumably ingested by the putative definitive hosts, skates and rays, which are expected to excrete Polypocephalus eggs. Images from the Noun Project https://thenounproject.com: shrimp by Jeffrey Qua, crab by Mallory Hawes, scallop by B Barrett, and skate by Örn Smári Gíslason, used under CC BY 3.0 license https://creativecommons.org/licenses/by/3.0/us/.

Figure 3. Infection patterns of sand crabs and mole crabs by parasites.

(A) Infection of crabs by unidentified nematode species. Lepidopa benedicti data redrawn from Joseph & Faulkes (2014). (B) Infection pattern of crabs by Polypocephalus sp. larvae. Summary statistics: square, mean; line dividing box, median; box, 50% of data; whiskers, 95% of data; triangles, minimum and maximum. Raw data shown by dots.

Figure 4. Micrographs of Polypocephalus sp. in nervous tissue.

(A) Lepidopa benedicti thoracic ganglion 2. (B) Lepidopa benedicti thoracic ganglia 3, and fused ganglion consisting of thoracic ganglia 4, 5, and abdominal ganglion 1. Different individual than (A). (C) Emerita benedicti brain. Arrow indicates single Polypocephalus larvae. (D) Emerita benedicti thoracic ganglion 1. No Polypocephalus sp. larvae in this individual. Different individual than (C). Anterior towards top in (A), and towards left in (B–D).

Figure 5. Bigger Lepidopa benedicti have more Polypocephalus sp. larvae.

Relationship between size of L. benedicti and intensity of Polypocephalus sp. infection.

Figure 6. Number of Polypocephalus sp. larvae in different regions of the nerve cord in Lepidopa benedicti.

Summary statistics: square, mean; line dividing box, median; box, 50% of data; whiskers, 95% of data; triangles, minimum and maximum. Raw data shown by dots. Groups sharing a letter do not differ significantly from each other. Sample sizes vary because some ganglia were damaged during dissection. SEG, subesophageal ganglion; T, thoracic ganglion; A, abdominal ganglion.

Figure 7. Polypocephalus sp. infection does not affect speed of digging in Lepidopa benedicti.

Relationship between intensity of Polypocephalus sp. infection and digging time in L. benedicti.

Figure 8. Size does not affect digging time in Lepidopa benedicti.

Relationship between carapace length and mean digging time in L. benedicti.

Figure 9. Time above sand for different behaviours by Lepidopa benedicti.

Duration of individual behaviour trials, grouped by different behaviours. N = 110 trials. Four trials involved combinations of sitting and swimming, and are not shown due to their rarity. Summary statistics: square, mean; line dividing box, median; box, 50% of data; whiskers, 95% of data; triangles, minimum and maximum. Raw data shown by dots. Groups sharing a letter do not differ significantly from each other.

Figure 10. Infection intensity of Lepidopa benedicti individuals showing different behaviours.

Individuals categorized into three groups: those that always dug directly; those that swam at least once, but never “sat” (i.e., remaining immobile on the surface); those that “sat” at least once, but never swam. Summary statistics: square, mean; line dividing box, median; box, 50% of data; whiskers, 95% of data; triangles, minimum and maximum. Raw data shown by dots. Groups sharing a letter do not differ significantly from each other.