Unravelling the trophic interaction between a parasitic barnacle (Anelasma squalicola) and its host Southern lanternshark (Etmopterus granulosus) using stable isotopes

Abstract

The parasitic barnacle, Anelasma squalicola, is a rare and evolutionary fascinating organism. Unlike most other filter-feeding barnacles, A. squalicola has evolved the capability to uptake nutrient from its host, exclusively parasitizing deepwater sharks of the families Etmopteridae and Pentanchidae. The physiological mechanisms involved in the uptake of nutrients from its host are not yet known. Using stable isotopes and elemental compositions, we followed the fate of nitrogen, carbon and sulphur through various tissues of A. squalicola and its host, the Southern lanternshark Etmopterus granulosus, to better understand the trophic relationship between parasite and host. Like most marine parasites, A. squalicola is lipid-rich and clear differences were found in the stable isotope ratios between barnacle organs. It is evident that the deployment of a system of ‘rootlets’, which merge with host tissues, allows A. squalicola to draw nutrients from its host. Through this system, proteins are then rerouted to the exterior structural tissues of A. squalicola while lipids are used for maintenance and egg synthesis. The nutrient requirement of A. squalicola was found to change from protein-rich to lipid-rich between its early development stage and its definitive size.

Keywords: Deepwater; New Zealand; food web; host–parasite; nitrogen; parasite; shark; stable isotopes; trophic position.

Graphical abstract

Fig. 1.

Map depicting the locations where Etmopterus granulosus infected with Anelasma squalicola were collected on Chatham Rise, New Zealand in January 2022. The number of parasitic barnacles and their site of infection on each host shark are indicated by the green ovals.

Fig. 2.

Anelasma squalicola in situ on Etmopterus granulosus. (A) Pre-dissection photograph of A. squalicola infecting E. granulosus (left) and partially dissected A. squalicola showing ‘unhealthy’ host tissue infested with A. squalicola rootlets, Pd, and healthy host tissue (H) (right). (B) Two parasitic barnacles (varying in size) illustrating tissues taken for stable isotope analyses. These include mouth, cirri and penis (MCP), eggs (Egg), mantle (M), peduncle (Pd) and rootlets (R). Not represented is the inner mantle, a soft tissue found within the mantle. Scale bars represent 1 cm.

Fig. 3.

(A) Anelasma squalicola in situ of the right eye of E. granulosus whereby rootlets appear to have penetrated host cartilage for access to host muscle in the centre of the shark head. (B) Visual characterization of A. squalicola identified as either protein-rich (purple) or lipid-rich (pink) tissues. (C) Stable isotope values and elemental compositions differences between parasite and host tissues. The difference between all barnacle ‘protein tissues’ (mean of all barnacles except individuals on shark no. 11 and their matching shark ‘healthy’ muscle tissues; green); the difference between shark no. 11′s barnacle ‘protein tissues’ and the eye tissue of the shark (grey); and the difference between shark no. 11 barnacle's ‘protein tissues’ and the ‘healthy’ shark muscle tissue (yellow).

Fig. 4.

Proposed physiological mechanisms behind parasitic barnacle feeding. (1) ‘Healthy’ shark muscle tissue, (2) ‘unhealthy’ shark tissue, (3) one of the barnacle's peduncle, (4) the same barnacle's protein tissues and (5) its egg stock. Green arrow represents a transfer of lipids and proteins via the barnacle's rootlets, orange arrow represents a transfer of proteins for maintenance and yellow arrow represents a transfer of lipids to the next generation.