Crustacean Research 2022 Vol.51: 111–113©Carcinological Society of Japan. doi: 10.18353/crustacea.51.0_111

First record of the maternal care behavior of a “rhizarian rider,”Phronimopsis spinifera Claus, 1879 (Amphipoda, Hyperiidea), inassociation with Aulosphaera sp. (Rhizaria, Cercozoa, Phaeodaria,Aulosphaeridae)
Nobuhiro Saito, Aiko Kayama, Yasuhide Nakamura
Rhizaria are a supergroup of unicellular eukaryotes, mainly composed of mineralized
skeleton-bearing protists such as Foraminifera,Radiolaria, and Phaeodaria (Nakamura et al.,2019a). Some species of rhizarians (Phaeodariaand Radiolaria) and crustaceans (Amphipodaand Decapoda) show a unique symbiotic relationship (Wakabayashi et al., 2017; Nakamura& Suzuki, 2019), called the “rhizarian rider”
phenomenon (Nakamura et al., 2019b). The association between Phronimopsis spinifera
Claus, 1879 (Amphipoda, Hyperiidea) and Aulosphaera sp. (Rhizaria, Phaeodaria) is themost commonly observed combination of rhizarian riders. Phronimopsis spinifera is a marine
pelagic amphipod species widely distributed in
the tropical regions of the Atlantic, Indian, andPaciﬁc oceans, as well as the Mediterranean
and Red Seas (Vinogradov et al., 1996). In the“rhizarian rider” phenomenon, P. spinifera carries 2–9 individuals of Aulosphaera sp. It has
been observed that P. spinifera holds rhizarians
using the chelae of the ﬁfth to seventh pereopods. The rhizarians carried by the amphipod
may function as food collectors and ﬂoats tokeep buoyancy (or to save the swimming energy of P. spinifera).
During our ﬁeld investigation by SCUBA
diving, a photograph of P. spinifera in association with Aulosphaera sp. was captured by oneof the authors (A. Kayama) using a digitalcamera (LUMIX DC-GX7MK3) (Fig. 1) on 3
June 2022 at a water depth of 8 m, 8 km westoﬀ the Ani-jima Island (N27°07′21″ E142°12′35″), Ogasawara Islands, in the western North
Paciﬁc. A mature female of P. spinifera (ca.

3 mm in body length) carrying 6 individuals ofAulosphaera sp. and 1–2 amphipod juveniles
attaching on the surface of or partly inside eachrhizarian individual are shown in the photograph. As these juveniles are similar in size andshape, they are likely at the same developmental stage.
In general, mature female amphipods spawn
in their brood pouches, wherein the embryos
hatch (Irie, 1967). Some species of Hyperiidea
raise their juveniles on the surface of or insidegelatinous zooplankton, such as doliolids,salps, and jellyﬁshes (some of them are known
as “barrel”) (Harbison et al., 1977; Madin &Harbison, 1977; Laval, 1980; Gasca & Haddock, 2004; Aoki et al., 2013; Gasca et al.,2015; Mazda et al., 2019).
In this study, it is revealed for the ﬁrst timethat rhizarian riders have similar maternal carebehavior, including demarsupication of theirprogeny on the symbiont. It is suggested thatamphipods utilize rhizarians not only as ﬂoats
and food collectors but also as breeding beds.
It is noteworthy that amphipod juveniles aredistributed over the whole rhizarian colony, as
if each juvenile holds its own rhizarian individual. This characteristic has never been reported
in other amphipods. The observed rhizariangroup, Aulosphaeridae, forms a colony of several individuals. After a speciﬁc time, rhizarian
individuals separate each other, becoming solitary individuals (e.g., Nakamura et al., 2017).
For amphipods, a colony of rhizarians is moreadvantageous than a solitary rhizarian as it prevents competition among amphipod juveniles
for rhizarians. Therefore, the mother amphi-Received: 14 Jul 2022. Accepted: 13 Sep 2022. Published online: 19 Oct 2022.

111

NOBUHIRO SAITO, AIKO KAYAMA, YASUHIDE NAKAMURA

Fig. 1. A photograph of “rhizarian rider,” a mature female of Phronimopsis spinifera (ca. 3 mm BL) (asterisk) carrying a colonyof Aulosphaera sp. (ﬁlled arrow heads). On the surface or partly inside of each rhizarian individual, 1–2 amphipod juveniles wereattached (opened arrow heads). The longest distance of the rhizarian colony was ca. 10 mm. Photo by Aiko Kayama.

pods may choose a colony of rhizarians to increase the survival of its juveniles. Furtherstudies are necessary to clarify the details of
the rhizarian rider phenomenon, including maternal care behavior; it needs to be investigatedwhether juvenile amphipods are identical, rhizarians are controlled (e.g., prevention of theirdispersal) by the mother amphipod, and juvenile amphipods feed on rhizarians or otherfood.

■ Acknowledgements
We wish to express our gratitude to Mr.
Hideki Abe (Hideki Abe Photo Oﬃce) for
helping us in the ﬁeld observation and provid112

Crustacean Research 51

ing valuable information. Thanks are also extended to Dr. Akira Asakura (Kyoto University), Editor-in-Chief of Crustacean Research,
and an anonymous reviewer for their constructive comments to our manuscript.

■ Literature Cited
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Association of the United Kingdom, 93(6):1553–1556. https://doi.org/10.1017/S0025315413000143

FIRST RECORD OF THE MATERNAL CARE BEHAVIOR OF A “RHIZARIAN RIDER”

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Addresses(NS) Suido-sha Co., Ltd., 8–11–11 Ikuta,Tama-ku, Kawasaki 214–0038, Japan(AK) Wako, Saitama, Japan(YN) Estuary Research Center, Shimane
University, 1060 Nishikawatsu-cho, Matsue
690–8504, JapanE–mail addresses(NS)* nsaitoh@suidosha.co.jp(YN) jasnakamura@gmail.com*Corresponding author

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