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. 2017 Sep 20;12(9):e0184311.
doi: 10.1371/journal.pone.0184311. eCollection 2017.

A new species of hermit crab, Diogenes heteropsammicola (Crustacea, Decapoda, Anomura, Diogenidae), replaces a mutualistic sipunculan in a walking coral symbiosis

Affiliations

A new species of hermit crab, Diogenes heteropsammicola (Crustacea, Decapoda, Anomura, Diogenidae), replaces a mutualistic sipunculan in a walking coral symbiosis

Momoko Igawa et al. PLoS One. .

Abstract

Symbiont shift is rare in obligate mutualisms because both the partners are reciprocally dependent on and specialized to each other. In the obligate accommodation-transportation mutualism between walking corals and sipunculans, however, an unusual saltatory symbiont shift was discovered. In shallow waters of southern Japan, an undescribed hermit crab species was found living in corallums of solitary scleractinian corals of the genera Heterocyathus and Heteropsammia, replacing the usual sipunculan symbiont. We described the hermit crab as a new species Diogenes heteropsammicola (Decapoda, Anomura, Diogenidae), and explored its association with the walking corals. This hermit crab species obligately inhabits the coiled cavity of the corals, and was easily distinguished from other congeneric species by the exceedingly slender chelipeds and ambulatory legs, and the symmetrical telson. Observations of behavior in aquaria showed that the new hermit crab, like the sipunculan, carries the host coral and prevents the coral from being buried. This is an interesting case in which an organism phylogenetically distant from Sipuncula takes over the symbiotic role in association with a walking coral. The hermit crab species is unique in that its lodging is a living solitary coral that grows with the hermit crab in an accommodation-transportation mutualism.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Diogenes heteropsammicola sp. nov.
A, paratype, male (sl. 1.3 mm), NSMT-Cr 25561; B–E, holotype, male (sl. 1.3 mm), NSMT-Cr 25560. A, shield and cephalic appendages, dorsal view (setae on left side omitted); B, left antennal flagellum, dorsal view; C, left third maxilliped, lateral view (setae omitted); D, dactylus, propodus, and distal part of carpus of left fourth pereopod, lateral view (setae omitted); E, telson, dorsal view. Scale bars: 0.5 mm.
Fig 2
Fig 2. Diogenes heteropsammicola sp. nov., holotype, male (sl 1.3 mm), NSMT-Cr 25560. Left cheliped.
A, chela, dorsal view; B, dactylus and fixed finger, ventral view; C, carpus, dorsal view; D, carpus and merus, lateral view; E, same, mesial view. Scale bar: 0.5 mm.
Fig 3
Fig 3. Diogenes heteropsammicola sp. nov., holotype, male (sl 1.3 mm), NSMT-Cr 25560. Right cheliped.
A, chela, dorsal view (setae omitted); B, entire, mesial view; C, same, lateral view (setae omitted); D, carpus, dorsal view (setae omitted). Scale bar: 0.5 mm.
Fig 4
Fig 4. Diogenes heteropsammicola sp. nov., holotype, male (sl 1.3 mm), NSMT-Cr 25560. Left second pereopod.
A, lateral view; B, mesial view (only setae on surface shown). Scale bar: 0.5 mm.
Fig 5
Fig 5. Diogenes heteropsammicola sp. nov., holotype, male (sl 1.3 mm), NSMT-Cr 25560. Left third pereopod.
A, lateral view; B, mesial view (only setae on surface shown). Scale bar: 0.5 mm.
Fig 6
Fig 6. Diogenes heteropsammicola sp. nov. in life.
A, an individual in an aquarium, carrying the coral; B, an individual removed from its host coral. Scale bar: 1 mm.
Fig 7
Fig 7. Behavior of Diogenes heteropsammicola sp. nov.
A–C, sequence of behaviors to recover from an overturned to upright position in which the hermit crab leans out of the overturned coral (A), grasps the bottom with its ambulatory legs and left cheliped (B), and turns the coral upright using the pleon (C); D–F, sequence of behaviors to overcome burial in sediment, whereby the buried hermit crab (D) pushes away the sediment using its chelipeds and ambulatory legs (E), and then crawls away (F).
Fig 8
Fig 8. Frequencies of solitary corals symbiotic with a hermit crab/sipunculan in Oshima Strait.
Number of solitary corals (Hc, Heterocyathus alternatus; Hp, Heteropsammia cochlea) inhabited by a hermit crab/sipunculan.
Fig 9
Fig 9. Frequencies of solitary corals having dextrally/sinistrally coiled cavities.
Number of solitary corals (Hc, Heterocyathus alternatus; Hp, Heteropsammia cochlea) having dextrally/sinistrally coiled cavities, in the case of hermit crab-occupied (A) and sipunculan-occupied (B) corals.

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