Mar Biodiv DOI 10.1007/s12526-017-0668-5 ORIGINAL PAPER Symbiotic associations of crustaceans and a pycnogonid with gelatinous zooplankton in the Gulf of California Rebeca Gasca1 & William E. Browne 2 Received: 6 June 2016 /Revised: 13 February 2017 /Accepted: 21 February 2017 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017 Abstract Symbiotic associations between pelagic arthropods Introduction and gelatinous zooplankters were surveyed and analyzed via blue-water SCUBA and a remotely operated submersible In the vast and relatively unstructured water column of the (ROV) during March 2015 in the Gulf of California. Our open ocean, all organisms can become potential host sub- analyses focused on hyperiid amphipods (10 species), cope- strates for other organisms. These interactions often manifest pods (1), and pycnogonids (1) associated with different groups in a wide variety of both casual and strict long-term relation- of gelata. Here. we report observations on 13 previously un- ships. In the largest contiguous habitat on the planet, organ- documented and 4 known symbiotic associations. The nature isms participating in such associations remain largely un- and dynamics of these associations are still poorly understood, known (Lützen 2005; Fleming et al. 2014), a knowledge gap particularly those involving deep-living taxa. The discovery of that impedes a fuller understanding of pelagic biology. This is the pycnogonid Bathypallenopsis calcanea (Stephensen, especially true among zooplankters, particularly those that 1933) in association with the medusa Aeginura grimaldii inhabit midwater and deep aphotic zones. Maas, 1904 was predicted by Hedgpeth (Deep-Sea Res The gelatinous zooplankton (gelata) community inhabiting 9:487–491, 1962). We include in vivo or in situ photographs the water column can occur at high abundance and typically of some of these associations. The Megalanceoloides,previ- includes organisms from several distinct phyla including ously reported as M. remipes (Barnard), are here recognized as Cnidaria, Ctenophora, Salpidae, and Mollusca. In comparison belonging to a new species. These new data represent a sig- with other abundant zooplankters, such as small- or medium- nificant addition to our knowledge of these symbiotic associ- sized crustaceans, the gelata often include relatively large an- ations in the mid- and deep waters of the Gulf of California. imals that become particularly good host targets. Many plank- tonic crustaceans have been described as parasites of gelata species; however, it is often not clear what potential benefits Keywords Symbiotic crustaceans . Deep-living are being gained from these putative host–symbiont associa- zooplankton . Hyperiid amphipods . New species . tions. For example, the hyperiid amphipods are known for a Symbioses . Gelata number of parasitoid interactions with a number of gelata hosts during at least part of their life history (Laval 1980), but in many cases the nature of these symbiotic associations Communicated by P. Martinez Arbizu remains vague (Dittrich 1988) or unknown. Therefore, these largely uncharacterized symbioses could encompass a wide * Rebeca Gasca range of interactions including, but not limited to, [email protected] ectoparasitism, endoparasitism, commensalism, and amensalism. 1 Unidad Chetumal, El Colegio de la Frontera Sur (ECOSUR), Av. del Most of our knowledge about marine zooplankton has been Centenario Km. 5.5, Chetumal, Quintana Roo C.P. 77014, Mexico obtained from sampling with a wide array of nets and similar 2 Cox Science Center, University of Miami, 1301 Memorial Drive, gear (Wiebe and Benfield 2003). However, net samples are Miami, FL 33146, USA especially poor for information about symbiotic associations Mar Biodiv that include gelata, as these soft-bodied forms are particularly associated with numerous pelagic gelata hosts. Among the prone to being lost or badly damaged during the sampling hosts, we collected five salp species, two ctenophore species, process. Since the advent of SCUBA and the development two narcomedusae, two siphonophores, and a pterotracheid of submersible technologies in recent decades, we have gained mollusc. Table 1 provides a summary of the associations the ability to observe zooplankton and soft-bodied gelata taxa found during this survey. in situ intensively and in greater detail. Pairing these technol- Phylum Arthropoda ogies with studies focused on better understanding oceanic Subphylum Crustacea Brünnich, 1772 midwater environments have facilitated not only the discovery Class Malacostraca Latreille, 1802 of new species but also the characterization of novel aspects of Order Amphipoda Latreille, 1816 symbiotic associations between organisms in pelagic environ- Suborder Hyperiidea Milne-Edwards, 1830 ments (Madin et al. 2013; Gasca et al. 2007, 2015a, b). Infraorder Physosomata Pirlot, 1929 Ecologically, symbiotic associations between organisms Superfamily Scinoidea Bowman & Gruner, 1973 are important. We are clearly in a nascent stage of describing Family Mimonectidae Bovallius, 1885 the range of host–symbiont associations present in oceanic Mimonectes loveni Bovallius, 1885 midwater environments along with the underlying biology Material examined: Adult female 24 mm, undissected, eth- of these associations and their potential effects on host popu- anol preserved, collected on Apolemia spp. 8 March 2015 at lations (Bray 2005; Boxshall 2005). Crustaceans can often be 2325 m depth (Fig. 1a) (ECO-CHZ 009358). Adult female found piggybacking on, or embedded within, the body of 24.5 mm undissected, ethanol preserved, collected on many different species of gelata. However, the nature of the Apolemia spp. 12 March 2015 at 2576 m depth (Table 1, symbiosis is not always immediately evident. Surveys explor- Fig. 1b) (ECO-CHZ-009361). A third specimen was found ing the biology, diversity, and ecology of midwater fauna in during this cruise 13 March 2015 at 2419 m depth and it the southern and central Gulf of California were conducted by was a free swimming gravid female 27 mm in length the Monterey Bay Aquarium Research Institute (MBARI) in (Fig. 1c) (ECO-CHZ-009359). 2015. Based on observations and collections of midwater fau- Remarks na with SCUBA diving and ROV, we describe a number of This is the first reported observation of this species in newly observed host–symbiont interactions between arthro- association with the siphonophore Apolemia sp. It has pods and gelata. previously been recorded as a symbiont of the medusa Solmissus sp. by Zeidler (2012). Mimonectes loveni is widely distributed in the world oceans (Vinogradov Methods et al. 1996); however, this represents the first record of Mimonectes loveni in Mexican waters (Atlantic and Collections and observations of midwater and deep-living Pacific). Only 2 of the 11 known species of Mimonectes zooplankton were made in the southern Gulf of California have been previously observed in the Gulf of California: and Eastern Pacific Ocean sites near the opening to the Gulf M. gaussi (Woltereck 1904), reported in association with of California during 7–16 March 2015 with the MBARI R/V ctenophores and M. sphaericus Bovallius, 1885, a symbi- Western Flyer and ROV Doc Ricketts. ROV sampling was ont of both siphonophores and medusae (Gasca et al. performed at a depth range of 200–3600 m to obtain meso- 2015a, b; Siegel-Causey 1982). A third species, and bathypelagic samples. Blue-water SCUBA diving was M. spandli Stephensen and Pirlot, 1931 has been recorded used to sample the upper 30 m of the water column. A com- in association with the trachymedusa Voragonema bination of digital photography and videography were used tatsunoko (Lindsay and Pages 2010). These data suggest when possible to document faunal associations. After in vivo that Mimonectes associates with distinctly different observations, arthropod symbionts were fixed and preserved groups of gelata. The degree of host specificity between in either 70% ETOH or 10% formalin. Associated host gelata different species of Mimonectes deserves further study. As specimens were also fixed in 10% formalin for further taxo- shown in the illustration (Fig. 1c), the free-swimming nomic examination. Voucher specimens were deposited in the specimen appears transparent except for the developing collection of zooplankton (ECO-CHZ) held at El Colegio de eggs; only three eggs (approximately 650 μmincircum- la Frontera Sur, Unidad Chetumal, Mexico. ference) were recovered. The foregut, midgut and hindgut of the individuals attached to siphonophores appeared to be filled with host tissue, suggesting the role of Results Mimonectes as an ectoparasite is likely to encompass a diverse range of gelata. During the cruise, we collected ten hyperiid amphipod spe- Infraorder Physosomata Pirlot, 1929 cies, a copepod, and a pycnogonid species symbiotically Superfamily Lanceoloidea Bowman & Gruner, 1973 Mar Biodiv Table 1 Symbionts of gelatinous zooplankters in epipelagic and deep waters of the Gulf of California (March 2015) including depth, geographic location, method of collection and notes on the symbiont Symbiont Host Depth m Datea Lat N Long W Collection method Obs on symbiont Brachyscelus crusculum Metcalfina hexagona 329 7 24°30.09′ 109°59.58 D721 S2 1 M B. crusculum Pterotrachea coronata 15 9 25°26.96′ 109°30.93 BWD 1 F, 1 OF, 1 M B. crusculum Salpa maxima 15 m 9 25°26.96′ 109°30.93 BWD 1 OF B. crusculum Rosacea cymbiformis 15 m 10 24°19′ 109°12 BWD 1 jF B. crusculum Cestum veneris 15 m 10 24°19′ 109°12 BWD 1 OF Hyperoche mediterranea Beroe cucumis 15 m 13 22°55′ 108°6.95 BWD 1 OF Lycaea pulex Salpa sp. 15 m 14 23°41.54′ 108°49 BWD 1 jF Megalanceoloides aequanime sp. nov. Apolemia sp. 2094 8 25°27′ 109°51 D722 D8 1 OF Mimonectes loveni Apolemia sp. 2325 8 25°27′ 109°51 D722 SS8 1 F M. loveni Apolemia sp. 2589 12 22°55′ 108°6.95 D726 SS6 1 F Parapronoe parva Rosacea cymbiformis 15 m 9 25°26.96′ 109°30.93 BWD 1 OF P. parva Rosacea cymbiformis 15 m 10 24°19′ 109°12 BWD 1 OF, 1 FB Prohyperia shihi Pegantha laevis 926 14 23°41.54′ 108°49 D728 DS10 2 jF? Vibilia antarctica Salpa maxima 440 7 24°30.09′ 109°59.58 D721 SS5 4 jF, 1 M V.