ORIGINAL PAPER

Symbiotic associations of crustaceans and a pycnogonidwith gelatinous zooplankton in the Gulf of California

Rebeca Gasca1 & William E. Browne2

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 arthropodsand gelatinous zooplankters were surveyed and analyzed viablue-water SCUBA and a remotely operated submersible(ROV) during March 2015 in the Gulf of California. Ouranalyses focused on hyperiid amphipods (10 species), cope-pods (1), and pycnogonids (1) associatedwith different groupsof gelata. Here. we report observations on 13 previously un-documented and 4 known symbiotic associations. The natureand dynamics of these associations are still poorly understood,particularly those involving deep-living taxa. The discovery ofthe pycnogonid Bathypallenopsis calcanea (Stephensen,1933) in association with the medusa Aeginura grimaldiiMaas, 1904 was predicted by Hedgpeth (Deep-Sea Res9:487–491, 1962). We include in vivo or in situ photographsof some of these associations. The Megalanceoloides, previ-ously reported asM. remipes (Barnard), are here recognized asbelonging to a new species. These new data represent a sig-nificant addition to our knowledge of these symbiotic associ-ations in the mid- and deep waters of the Gulf of California.

Keywords Symbiotic crustaceans . Deep-livingzooplankton . Hyperiid amphipods . New species .

Symbioses . Gelata

Introduction

In the vast and relatively unstructured water column of theopen ocean, all organisms can become potential host sub-strates for other organisms. These interactions often manifestin a wide variety of both casual and strict long-term relation-ships. In the largest contiguous habitat on the planet, organ-isms participating in such associations remain largely un-known (Lützen 2005; Fleming et al. 2014), a knowledge gapthat impedes a fuller understanding of pelagic biology. This isespecially true among zooplankters, particularly those thatinhabit midwater and deep aphotic zones.

The gelatinous zooplankton (gelata) community inhabitingthe water column can occur at high abundance and typicallyincludes organisms from several distinct phyla includingCnidaria, Ctenophora, Salpidae, and Mollusca. In comparisonwith other abundant zooplankters, such as small- or medium-sized crustaceans, the gelata often include relatively large an-imals that become particularly good host targets. Many plank-tonic crustaceans have been described as parasites of gelataspecies; however, it is often not clear what potential benefitsare being gained from these putative host–symbiont associa-tions. For example, the hyperiid amphipods are known for anumber of parasitoid interactions with a number of gelatahosts during at least part of their life history (Laval 1980),but in many cases the nature of these symbiotic associationsremains vague (Dittrich 1988) or unknown. Therefore, theselargely uncharacterized symbioses could encompass a widerange of interactions including, but not limited to,ectoparasitism, endoparasitism, commensalism, andamensalism.

Most of our knowledge about marine zooplankton has beenobtained from sampling with a wide array of nets and similargear (Wiebe and Benfield 2003). However, net samples areespecially poor for information about symbiotic associations

Communicated by P. Martinez Arbizu

* Rebeca Gascargasca@ecosur.mx

1 Unidad Chetumal, El Colegio de la Frontera Sur (ECOSUR), Av. delCentenario Km. 5.5, Chetumal, Quintana Roo C.P. 77014, Mexico

2 Cox Science Center, University of Miami, 1301 Memorial Drive,Miami, FL 33146, USA

Mar BiodivDOI 10.1007/s12526-017-0668-5

that include gelata, as these soft-bodied forms are particularlyprone to being lost or badly damaged during the samplingprocess. Since the advent of SCUBA and the developmentof submersible technologies in recent decades, we have gainedthe ability to observe zooplankton and soft-bodied gelata taxain situ intensively and in greater detail. Pairing these technol-ogies with studies focused on better understanding oceanicmidwater environments have facilitated not only the discoveryof new species but also the characterization of novel aspects ofsymbiotic associations between organisms in pelagic environ-ments (Madin et al. 2013; Gasca et al. 2007, 2015a, b).

Ecologically, symbiotic associations between organismsare important. We are clearly in a nascent stage of describingthe range of host–symbiont associations present in oceanicmidwater environments along with the underlying biologyof these associations and their potential effects on host popu-lations (Bray 2005; Boxshall 2005). Crustaceans can often befound piggybacking on, or embedded within, the body ofmany different species of gelata. However, the nature of thesymbiosis is not always immediately evident. Surveys explor-ing the biology, diversity, and ecology of midwater fauna inthe southern and central Gulf of California were conducted bythe Monterey Bay Aquarium Research Institute (MBARI) in2015. Based on observations and collections of midwater fau-na with SCUBA diving and ROV, we describe a number ofnewly observed host–symbiont interactions between arthro-pods and gelata.

Methods

Collections and observations of midwater and deep-livingzooplankton were made in the southern Gulf of Californiaand Eastern Pacific Ocean sites near the opening to the Gulfof California during 7–16 March 2015 with the MBARI R/VWestern Flyer and ROV Doc Ricketts. ROV sampling wasperformed at a depth range of 200–3600 m to obtain meso-and bathypelagic samples. Blue-water SCUBA diving wasused to sample the upper 30 m of the water column. A com-bination of digital photography and videography were usedwhen possible to document faunal associations. After in vivoobservations, arthropod symbionts were fixed and preservedin either 70% ETOH or 10% formalin. Associated host gelataspecimens were also fixed in 10% formalin for further taxo-nomic examination. Voucher specimens were deposited in thecollection of zooplankton (ECO-CHZ) held at El Colegio dela Frontera Sur, Unidad Chetumal, Mexico.

Results

During the cruise, we collected ten hyperiid amphipod spe-cies, a copepod, and a pycnogonid species symbiotically

associated with numerous pelagic gelata hosts. Among thehosts, we collected five salp species, two ctenophore species,two narcomedusae, two siphonophores, and a pterotracheidmollusc. Table 1 provides a summary of the associationsfound during this survey.

Phylum ArthropodaSubphylum Crustacea Brünnich, 1772Class Malacostraca Latreille, 1802Order Amphipoda Latreille, 1816Suborder Hyperiidea Milne-Edwards, 1830Infraorder Physosomata Pirlot, 1929Superfamily Scinoidea Bowman & Gruner, 1973Family Mimonectidae Bovallius, 1885Mimonectes loveni Bovallius, 1885Material examined: Adult female 24 mm, undissected, eth-

anol preserved, collected on Apolemia spp. 8 March 2015 at2325 m depth (Fig. 1a) (ECO-CHZ 009358). Adult female24.5 mm undissected, ethanol preserved, collected onApolemia spp. 12 March 2015 at 2576 m depth (Table 1,Fig. 1b) (ECO-CHZ-009361). A third specimen was foundduring this cruise 13 March 2015 at 2419 m depth and itwas a free swimming gravid female 27 mm in length(Fig. 1c) (ECO-CHZ-009359).

RemarksThis is the first reported observation of this species in

association with the siphonophore Apolemia sp. It haspreviously been recorded as a symbiont of the medusaSolmissus sp. by Zeidler (2012). Mimonectes loveni iswidely distributed in the world oceans (Vinogradovet al. 1996); however, this represents the first record ofMimonectes loveni in Mexican waters (Atlantic andPacific). Only 2 of the 11 known species of Mimonecteshave been previously observed in the Gulf of California:M. gaussi (Woltereck 1904), reported in association withctenophores and M. sphaericus Bovallius, 1885, a symbi-ont of both siphonophores and medusae (Gasca et al.2015a, b; Siegel-Causey 1982). A third species,M. spandli Stephensen and Pirlot, 1931 has been recordedin association with the trachymedusa Voragonematatsunoko (Lindsay and Pages 2010). These data suggestthat Mimonectes associates with distinctly differentgroups of gelata. The degree of host specificity betweendifferent species of Mimonectes deserves further study. Asshown in the illustration (Fig. 1c), the free-swimmingspecimen appears transparent except for the developingeggs; only three eggs (approximately 650 μm in circum-ference) were recovered. The foregut, midgut and hindgutof the individuals attached to siphonophores appeared tobe filled with host tissue, suggesting the role ofMimonectes as an ectoparasite is likely to encompass adiverse range of gelata.

Infraorder Physosomata Pirlot, 1929Superfamily Lanceoloidea Bowman & Gruner, 1973

Mar Biodiv

Family Megalanceolidae Zeidler, 2009Megalanceoloides aequanime sp. nov. GascaMegalanceoloides remipes (Barnard, 1932), Gasca and

Haddock (2016)Material examined: One ovigerous female, length 25 mm,

undissected, ethanol-preserved, collected 8 March 2015 at adepth of 2094 m (Fig. 1d) (ECO-CHZ 009312).

RemarksA description and a detailed morphological comparison of

this species was provided by Gasca and Haddock (2016) whofound differences with respect to the known populations ofM.remipes and attributed them to intraspecific variation. Thesedifferences were confirmed in the specimen examined here,and it is considered that these differences, together with thegeographic range ofM. remipes, is enough evidence to recog-nize the Californian specimen (Gasca and Haddock 2016) asrepresentative of a new species, which is here named as M.aequanime sp. nov., which is made available. The specimenfrom the Gulf of California (Gasca and Haddock, 2016)should be deemed the holotype. The specimen examined inthis survey was found on the siphonophore Apolemia sp.; it

was clearly a symbiont on the siphonophore, firmly clingingto its siphosome (Fig. 1d). It was previously reported byGascaand Haddock (2016) as the first record of a symbiotic associ-ation of the family and is one of the few (only 5 known to date)reports involving members of the Superfamily Lanceoloidea,a group currently containing 7 families, 9 genera and 39species.

Infraorder Physocephalata Bowman and Gruner, 1973Family Vibiliidae Dana, 1852Vibilia antarctica Stebbing, 1888Material examined: Four juvenile females and a juvenile

male (sizes 6.6–11 mm) collected during Dive 721-S5 on 7March 2015 at 440 m depth from a chain (20 individuals) ofSalpa maxima Forskål, 1775 with a total of 41 V. antarcticaassociated with both the external and internal surfaces of thehost salp (ECO-CHZ 009367). Female V. antarctica (13 mm)(Fig. 1e) (ECO-CHZ 009364) fixed in ethanol, collected inassociation with Cyclosalpa bakeri Ritter, 1905 at 15 m depthby blue-water SCUBA diving, 10 March 2015. Juvenile maleand 11 juvenile females (sizes 8.8–10 mm) (ECO-CHZ009365) fixed and preserved in ethanol, collected during

Table 1 Symbionts of gelatinous zooplankters in epipelagic and deep waters of the Gulf of California (March 2015) including depth, geographiclocation, 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. antarctica 28 Cyclosalpa bakeri 15 m 10 24°19′ 109°12 BWD 1 F

V. antarctica 41 Ritteriella picteti 651 11 23°37′ 108°45 D725 SS6 1 jM, 11 jF

V. antarctica M. hexagona 315 11 23°37′ 108°45 D725 SS7 2 j

Vibilia gibbosa S. maxima 266 7 24°30.09′ 109°59.58 D721 SS8 7 j F?

V. longicarpus M. hexagona 249 11 23°37′ 108°45 D725 SS9 1 jM

V. longicarpus M. hexagona 315 11 23°37′ 108°45 D725 SS7 1 M

Sapphirina sinuicauda M. hexagona 15 m 12 22°55′ 108°6.95 BWD 1 M

Bathypallenopsis calcanea Aeginura grimaldii 2300 14 23°41.54′ 108°49 D728-DS3 Pycnogonid

BWD blue-water SCUBA, B with brood, D ROV dive, F female, j juvenile, M male, OF ovigerous female, SS suction sampleraMarch 2015

Mar Biodiv

Dive 725-S6 on 11 March 2015 at 651 m depth, together withthe salp Ritteriella picteti (Apstein, 1904); salp fixed in for-malin. Two juveniles (7 and 8.2 mm) (ECO-CHZ 009366)collected from the salp Metcalfina hexagona (Quoy &Gaimard, 1824) during Dive 725-S7 at 315 m depth, 11March2015, fixed and preserved in formalin.

RemarksThis hyperiid species is known to be distributed south of

the Subtropical Convergence. In the Eastern Pacific, it hasbeen recorded from Peruvian waters but can be transportedby oceanic currents to higher latitudes. It is reported as rare

in the Gulf of California and has been collected only at night-time (Siegel-Causey 1982). Occurrences in the Gulf could berelated to the local influence of Pacific Intermediate Watersthat lie at 500 m and are linked to the Antarctic (Trasviña et al.1999). Presence in surface waters may be due to diel migrationpatterns of the host salp. Overall, this record could be consid-ered as the first being outside the known northern range ofV. antarctica. While these specimens may represent a distinctspecies, no morphological differences were detected with re-spect to Vinogradov’s et al. (1996) description and illustra-tions. Genetic analyses will be carried out to test this

Fig 1 a Mimonectes loveni withApolemia sp. b another specimenof Mimonectes loveni withApolemia sp. c Free-swimminggravid female ofMimonectesloveni. d Female ofMegalanceoloides aequanime sp.nov. (as M. remipes in Gasca andHaddock 2016) associated withApolemia sp. e Vibilia antarcticawith Salpa maxima. f Vibiliaantarctica with long chain ofRitteriella picteti (upper left insetmagnified view). g Vibiliagibbosa with Salpa maxima

Mar Biodiv

hypothesis and determine the taxonomic status of the Gulfpopulation. Vibilia antarctica has been recorded as a commonsymbiont of salps and this species along with their salp hostswere the most frequently observed symbiotic associations dur-ing this survey. With regard to distribution on their host, theyare highly abundant inside the host salp often associated withthe gill bar and/or nucleus (gut). For example we encountereda R. picteti salp chain of ∼70 individuals measuring 110 cmlong hosting more than 100 Vibilia antarctica (Fig. 1f). Vibiliaantarctica has been previously recorded associated with othersalps including Ihlea racovitzai and Salpa thompsoni (Phlegeret al. 2000). The specimen collected from a solitaryCyclosalpa bakeriwas observed in situ actively feeding whilemoving over the salp surface and extracting small fragmentsof salp tissue using the dactylae of its gnathopods.

Vibilia longicarpus Behning, 1913Material examined: Adult male, 12 mm, collected at 315 m

depth on the salpMetcalfina hexagona (Dive 725-S7) (ECO-CHZ 009370); adult male, 12 mm, collected at 249 m depthalso on M. hexagona (Dive 725-S9) (ECO-CHZ 009371),both specimens collected 11 March 2015.

RemarksThis is the first record of a symbiotic association for this

species with other zooplankters. One of the V. longicarpusmales was coexisting in the same salp host along with juvenilespecimens of V. antarctica.

Vibilia gibbosa Bovallius, 1887Material examined: Seven juvenile specimens (aprox.

5 mm), probably females, on S. maxima, collected at 266 m(Dive 721-S8), 7 March 2015 (Fig 1g) (ECO-CHZ 009368).

RemarksA chain of 19 individual S. maxima salps harboring 44

hyperiids was observed. Vibilia gibbosa were observedcrawling and feeding both inside the salps and on their exter-nal surfaces. This species has only been recorded associatedwith salps of the genus Salpa: S. fusiformis and S. aspera(Behning 1927). Fifteen of the nineteen known species ofVibilia have been recorded in association with salps. Vibiliahave not been associated with any other group of gelata.Additionally, most species of Vibilia have been found associ-ated with more than one species of salp. Only Vibiliajeangerardi Lucas, 1845 is known to occur in association witha single salp species: S. maxima (Marion 1874; Chevreux1892; Madin and Harbison 1977; Laval 1980).

Superfamily Phronimoidea Bowman & Gruner, 1973Family Hyperiidae Dana, 1852Hyperoche mediterranea Senna, 1908Material examined: One ovigerous female, 3.2 mm length,

collected by blue-water SCUBA at a depth of 15 m, 13March 2015, associated with the ctenophore Beroe cucumisFabricius, 1780 (Fig. 2a) (ECO-CHZ 009356).

RemarksThis is the first record of this species in the Gulf of

California associated with B. cucumis (Gasca et al. 2015a,b). Harbison et al. (1977) also recorded this observation inthe Caribbean Sea. The hyperiid H. mediterranea is a speciesknown to have a wide host range among gelata. It has beenrecorded associated mainly with ctenophores (Senna 1906;Steuer 1911; Hirota 1974; Flores and Brusca 1975; Harbisonet al. 1977, 1978; Laval 1980; Brusca 1981; Hoogenboom andHennen 1985; Gasca et al. 2015a, b) but also observed inassociation with siphonophores (Senna 1906) and medusae(Senna 1906; Brusca 1981; Gasca et al. 2015a, b). The varietyof host-symbiont interactions ofHyperoche mediterranea andHyperia medusarum are among the best documented amongthe Hyperiidae.

Prohyperia shihi (Gasca, 2005)Material examined: Two immature specimens, about

4.5 mm, collected from the medusa Pegantha laevisBigelow, 1909, 14 March 2015, depth 926 m (Fig. 2b, c)(ECO-CHZ 009363).

RemarksThis species, originally described from specimens collected

in the Gulf of California (Gasca 2005) was until recentlyknown only from a single female (Gasca 2013). During thissurvey, P. shihiwas found in association withPegantha laevis,expanding its known host range. This species has been record-ed at depths between 554 and 1136 m depth and appears to bea symbiont associated with a number of other medusae includ-ing the leptomedusa Chromatonema erythrogonon (Gasca2005), Nausithoe rubra (Gasca 2013) and Aegina citrea(Gasca et al. 2015a, b).

Superfamily Platysceloidea Bowman & Gruner 1973Family Pronoidae Claus, 1879Parapronoe parva Claus, 1879Material examined: One ovigerous female, 7.6 mm, with at

least 110 offspring of 0.8 mm, collected at a depth of 15 m, 9March 2015 (ECO-CHZ 009362), from the siphonophoreRosacea cymbiformis. Two additional specimens, one9.1 mm, with 52 offspring of 0.640 mm, and the other10.8 mm, a female carrying more than 100 eggs, 0.4 mmdiameter, collected 10 March 2015 (ECO-CHZ 009360), bothassociated with R. cymbiformis. All three specimens were col-lected by blue-water SCUBA.

RemarksPreviously, this species has been reported in association

with the siphonophore Rosacea cymbiformis (Delle Chiaje1830) in the central west and northwestern Atlantic(Harbison et al. 1977, as Sympronoe parva). Our observationsin the Gulf of California support the likely preferred associa-tion of P. parva with this siphonophore species. The speci-mens collected on March 10 were also found to be co-

Mar Biodiv

occurring on the same siphonophore host with Brachysceluscrusculum.

Family Lycaeidae Claus, 1879Lycaea pulex Marion, 1874Material examined: One young female of 4 mm, collected

from a salpCyclosalpa? at a depth of 15m,14March, by blue-water SCUBA (ECO-CHZ 009357).

RemarksThis is another species known to have a wide host range

among salps, it has been observed associated with no less thana dozen of different Thaliaceans (Marion 1874; Chevreux1892, 1900; Chevreux and Fage 1925; Pirlot 1939;Trégouboff and Rose 1957; Harbison 1976; Madin andHarbison 1977; Laval 1980; Hoogenboom and Hennen1985). In the Gulf of California we observed L. pulex in asso-ciation with a young solitary salp, likely Cyclosalpa?

Family Brachyscelidae Stephensen, 1923Brachyscelus crusculum Bate, 1861Material examined: One male, 7.5 mm, on the salp

Metcalfina hexagona (Quoy & Gaimard, 1824) collected at

329 m, 7 March 2015 (Fig. 2d) (ECO-CHZ 009351). Onefemale, (9.6 mm) an ovigerous female (7.6 mm), and an adultmale (8.6 mm) collected on the heteropod molluscPterotrachea coronata Forskål and Niebuhr, 1775 at 15 m,by blue-water SCUBA, 9 March 2015 (ECO-CHZ 009352).One ovigerous female (8.5 mm) collected associated with thesalp S. maxima, 15 m, 9 March 2015 (ECO-CHZ 009353).One juvenile female (5.6 mm), collected associated with thesiphonophore R. cymbiformis, 15 m, 10 March 2015 (ob-served co-occurring with P. parva) (ECO-CHZ 009354).One ovigerous female (10 mm, carrying 197 eggs) associatedwith the ctenophore Cestum veneris Lesueur, 1813, 15 cmlong, 10 March 2015 (ECO-CHZ 009355).

RemarksThis hyperiid is a known symbiont of a variety of gelata

taxa including; salps (Stephensen 1923; Madin and Harbison1977; Laval 1980), medusae (Pirlot 1939; Harbison et al.1977; Gasca and Haddock 2004), and also the pelagic mol-luscs Pterotrachea sp. (Harbison et al. 1977) andP. hippocampus (Gasca and Haddock 2004). It has not been

Fig 2 aHyperoche mediterraneawith Beroe cucumis. bProhyperia shihi with Peganthasp. view of medusa withamphipods, in situ. c Oralmagnified view of Peganthasp. associated with Prohyperiashihi. d Brachyscelus crusculumwith Metcalfina hexagona. eBathypallenopsis calcanea withAeginura grimaldi, lateral andsemi-oral views

Mar Biodiv

previously recorded from Metcalfina hexagona, thus our ob-servations expand the known host range of this species amongsalps.

Subclass Copepoda Milne-Edwards, 1840Order Poecilostomatoida Burmeister, 1835Family Sapphirinidae Thorell, 1859Sapphirina sinuicauda Brady, 1883Material examined: One adult female, collected on the salp

Metcalfina hexagona at 15 m, by blue-water SCUBA, 12March 2015 (ECO-CHZ 009372).

RemarksCopepods of the genus Sapphirina Thompson, 1829 have

been known as predators of salps since the first report ofsymbiotic association by Dana (1849). There are studiesconfirming females as specialized predators of salps that alsosuggest males use the salps for refuge (Takahashi et al. 2013).A male of this species had been previously recorded in theGulf of California from the salp Pegea confoederata (Forskål1775), not as a predator but only attached to the salp, possiblywaiting for a female (Gasca et al. 2015a, b). Our observationof a female on M. hexagona expands the host range ofS. sinuicauda in the Gulf of California.

Subphylum Chelicerata Heymons, 1901Class Pycnogonida Latreille, 1810Order Pantopoda Gerstaecker, 1863Family Pallenopsidae Fry, 1978Bathypallenopsis Stock, 1974Bathypallenopsis calcanea (Stephensen, 1933)Material examined. One specimen from Aeginura

grimaldii Maas, 1904, collected at a depth of 2300 m, 14March 2015 (Fig. 2e, f) (ECO-CHZ 009373).

RemarksBathypallenid pycnogonids are all considered bathype-

lagic forms associated with gelatinous organisms likescyphomedusae and doliolids (Bamber 2002), but in siturecords are very rare. Bathypallenopsis calcaneus was thefirst pycnogonid species to be recognized by Hedgpeth(1962) as a bathypelagic species among the more than500 described species of pycnogonids. Hedgpethsuspected they should be parasites or commensals associ-ated with larger organisms like medusae; he even sug-gested that the color of the medusae would be brownishmaroon because of residual pigments on the body of thepycnogonid. Hedgpeth proposed a probable associationwith Aeginura grimaldii because they had both been col-lected from the same sampling site. To date, only ninespecies of pycnogonids have been actually been observedparasitizing medusae (Pagès et al. 2007). Evidence of par-asitism or predation was provided by Child and Harbison(1986) with their observation of feeding on medusae tis-sue and tentacles; however, this kind of evidence has notalways been observed. Our sampling recovered a symbi-ont–host pair in which the host medusa seems to be

undamaged (Fig 2e, f). B. calcanea is a bathypelagic spe-cies recorded at a depth range of 353–8400 m (Turpaevaand Raiskii 2014). Mauchline (1984) accepted Hedgpeth’s(1962) suggestion of a cosmopolitan distribution forB. calcanea, and is currently deemed a widespread inhab-itant of both the Atlantic and Pacific ocean basins (Raiskiiand Turpaeva 2006). Our observations are the first recordof B. calcanea in the Gulf of California.

Discussion

Pelagic ecosystems occupy ∼95% of the biosphere yetremain one of the least studied habitats on earth. Pelagicecosystems are unique in that they lack solid substrate forhabitat, thus many species have adapted to a pelagic en-vironment by forming associations with other organisms.While these communities, composed primarily of arthro-pods and a variety of gelatinous organisms, are bothephemeral and patchy, it is noteworthy that new andknown associations between pelagic arthropods and gelat-inous zooplankters are consistently found during everysampling experiment, from the surface waters accessiblevia blue-water SCUBA through deeper depths accessiblevia ROV (Gasca and Haddock 2004; Gasca et al. 2007,2015a, b). Our campaign in the Gulf of California was noexception. To date, in the Gulf of California, there are 125described species of hyperiid amphipods. Among these,association data only exist for only 36 (29%) species.Thus, our observations serve to highlight the substantialknowledge gaps we currently face in efforts to describeand understand what are clearly ubiquitous biological re-lationships between pelagic arthropods and gelatinouszooplankters in oceanic mid-waters.

Despite discussions about hyperiid-gelata, symbiont–hostassociations in the literature for decades, it is clear that thesesymbioses cannot be described simply or accurately as para-sitism, phoresis, or commensalism. Certainly among thehyperiid amphipods, no single mode of symbiosis appears toprevail. In some cases, the association relationship is clearlydetrimental to the host, whereas in others the cost–benefits ofthe association to either the symbiont or host are not so clear.A number of parameters need further investigation to betterinform the underlying biology of these in situ observations,including but not limited to observations on the duration ofsymbiont–host associations, important additional observa-tions on parental behaviors associated with various symbio-ses, and more information on the degree of symbiont–hostspecificity.

Important biological questions about the nature of thesesymbiotic associations will only be revealed by the integrationof these data with past and future in situ observations of theseorganisms which play key roles in critically important oceanic

Mar Biodiv

food webs, and additionally may serve as key indicators ofmajor environmental perturbations. It is expected that futuresurveys will continue to expand our knowledge of pelagicsymbioses and aspects of the biology driving associations inzooplankton ecosystems.

Acknowledgements To Steven H.D. Haddock (chief scientist) for theinvitation to participate in the cruise to the Gulf of California, and to thecrew of the R/VWestern Flyer and the pilots and technicians of the ROVDoc Ricketts, whose invaluable work has allowed the discovery of theseand many other symbioses in the pelagic realm. To Gabriel Genzano,Alejandro Puente Tapia, Universidad Nacional de Mar del Plata andGeorge Matsumoto, MBARI for their help in the identification of medu-sae. Material was collected under permit DGOPA.-02919/14 issued bythe Mexican Ministry of Agriculture, Livestock, Rural Development,Fisheries and Food (SAGARPA). The scientific expeditionwas organizedand supported by the Monterey Bay Aquarium Research Institute(MBARI) and the David and Lucile Packard Foundation.

Compliance with Ethical Standards The Monterey Bay AquariumResearch Institute (MBARI) organized and the David and LucilePackard Foundation supported the scientific expedition. Rebeca Gascaand William Browne have no conflicts of interest involved in the devel-opment of this work. All applicable international, national, and/or insti-tutional guidelines for the care and use of animals were followed. Thisarticle does not contain any studies with human participants performed byany of the authors.

References

Bamber RN (2002) Bathypelagic pycnogonids (Arthropoda,Pycnogonida) from the discovery cruises. J Nat Hist 36:715–727

Bray RA (2005) Deep-sea parasites. In: Rhode K (ed) Marine parasitol-ogy. CSIRO, Collingwood, pp 366–370

Boxshall G (2005) Copepoda (copepods). In: Rhode K (ed) Marine par-asitology. CSIRO, Collingwood, pp 123–137

Brusca GJ (1981) A reexamination of some hyperiid amphipods fromHawaii. Pac Sci 34:227

Chevreux E (1892) Vibilia erratica, amphipode pélagique nouveau dulittoral des Alpes Maritimes. Bull Soc Zool Fr 16:32–35

Chevreux E (1900) Amphipodes provenant des campagnes del’BHirondelle^ (1885-1888). Rés Camp Sci Monaco 16:i–iv, 1–196, pl. 1–18

Chevreux E, Fage L (1925) Amphipodes. Faune Fr 9:1–488Child AC, Harbison GR (1986) A parasitic association between a pycno-

gonid and a scyphomedusa in midwater. J Mar Biol Assoc UK 66:113–117

Dana JD (1849) Conspectus Crustaceorum quæ in orbis Terrarumcircumnavigatione, Carolo Wilkes e Classe Reipublicæ Fœderatæduce, lexit et descripsit Jacobus D. Dana. Pars II. Proc Am AcadArts Sci 2:9–61

Dittrich B (1988) Studies on the life cycle and reproduction of the parasiticamphipodHyperia galba in the North Sea. HelgolMeeresun 42:79–98

Fleming NEC, Harrod C, Griffin DC, Newton J, Houghton JDR (2014)Scyphozoan jellyfish provide short-term reproductive habitat forhyperiid amphipods in a temperate near-shore environment. MarEcol Prog Ser 510:229–240

Flores M, Brusca GJ (1975) Observations on two species of hyperiidamphipods associated with the ctenophore Pleurobrachia bachei.Bull South Calif Acad Sci 74:10–15

Gasca R (2005) Hyperoche shihi sp. nov. (Crustacea: Peracarida:Amphipoda) a symbiont of a deep-living medusa in the Gulf ofCalifornia. J Plankton Res 27:617–621

Gasca R (2013) The male of the deep-living hyperiid Hyperoche shihiGasca, 2005 (Peracarida: Amphipoda) and a new symbiotic associ-ation in the Gulf of California. Crustaceana 86:1539–1549

Gasca R, Haddock SHD (2004) Associations between gelatinous zoo-plankton and hyperiid amphipods (Crustacea: Peracarida) in theGulf of California. Hydrobiologia 530(531):529–535

Gasca R, Haddock SHD (2016) The rare deep-living hyperiid amphipodMegalanceoloides remipes (Barnard, 1932): complementary de-scription and symbiosis. Zootaxa 4178(1):138–144

Gasca R, Suárez-Morales E, Haddock SHD (2007) Symbiotic associa-tions between crustaceans and gelatinous zooplankton in deep andsurface waters off California. Mar Biol 151:233–242

Gasca R, Hoover R, Haddock SHD (2015a) New symbiotic associationsof hyperiid amphipods (Peracarida) with gelatinous zooplankton indeep waters off California. J Mar Biol Assoc UK 95:503–511

Gasca R, Suárez-Morales E, Haddock SHD (2015b) Sapphirina irisDana, 1849 and S. sinuicauda Brady, 1883 (Copepoda,Cyclopoida) predators of salps in Monterey Bay and the Gulf ofCalifornia. Crustaceana 88:689–699

Harbison GR (1976) Development of Lycaea pulex Marion, 1874 andLycaea vincentii Stebbing, 1888 (Amphipoda, Hyperiidea). BullMar Sci 26:152–164

Harbison GR, Biggs DC, Madin LP (1977) The associations ofAmphipoda Hyperiidea with gelatinous zooplankton II.Associations with Cnidaria, Ctenophora and Radiolaria. Deep-SeaRes 24:465–488

Harbison GR,Madin LP, Swanberg NR (1978) On the natural history anddistribution of oceanic ctenophores. Deep-Sea Res 25:233–256

Hedgpeth JW (1962) A bathypelagic pycnogonid. Deep-Sea Res 9:487–491Hirota J (1974) Quantitative natural history of Pleurobrachia bachei in

La Jolla Bight. Bull US Br Fish 72:295–335Hoogenboom J, Hennen J (1985) Etude sur les parasites du

macrozooplankton gélatineux dans la Rade de Villefranche-sur-Mer (France), avec description des stades de développement deHyperoche mediterranea Senna (Amphipoda, Hyperiidae).Crustaceana 49:233–243

Laval P (1980) Hyperiid amphipods as crustacean parasitoids associatedwith gelatinous zooplankton. OceanogrMar Biol Annu Rev 18:11–56

Lindsay D, Pages F (2010) Voragonema tatsunoko (Trachymedusae:Rhopalonematidae), a new species of benthopelagic medusa, hostto the hyperiid amphipod Mimonectes spandli (Physosomata:Mimonectidae): Zootaxa. 2671:31–39

Lützen J (2005) Amphipoda (amphipods). In: Rohde K (ed) Marine par-asitology. CSIRO, Melbourne, pp 165–169

Madin LP, Harbison GR (1977) The associations of AmphipodaHyperiidea with gelatinous zooplankton. I. Associations withSalpidae. Deep-Sea Res 24:449–463

Madin LP, Hamner WM, Haddock SHD, Matsumoto GI (2013) Scubadiving in blue water: a window on ecology and evolution in theepipelagic ocean. Smithson Contrib Mar Sci 39:71–82

Marion AF (1874) Recherches sur les animaux inférieurs du golfe deMarseille. Deuxième mémoire. Description des CrustacésAmphipodes parasites des salpes. Ann Sci Nat Zool Biol Anim 6:1–19, pl 1–2

Mauchline J (1984) Pycnogonids caught in bathypelagic samples from theRockall Trough, northeastern Atlantic Ocean. J Nat Hist 18:315–322

Pagès FJ, Corbera J, Lindsay D (2007) Piggybacking pycnogonids andparasitic narcomedusae on Pandea rubra (Anthomedusae,Pandeidae). Plankton Benthos Res 2:83–90

Phleger CF, Nelson MM, Mooney B, Nichols PD (2000) Lipids ofAntarctic salps and their commensal hyperiid amphipods. PolarBiol 23:329–337

Mar Biodiv

Pirlot J-M (1939) Sur des Amphipodes Hypérides provenant des Croisièresdu Prince Albert 1er de Monaco. Res Camp Sci Monaco 102:1–63

Raiskii AK, Turpaeva EP (2006) Deep-sea pycnogonids from the northAtlantic and their distribution in the World Ocean. Oceanology 46:57–62

Senna A (1906) Su alcuni anfipodi iperini del plancton di Messina. BollSoc Entomol Ital 38:153–175

Siegel-Causey D (1982) Factors determining the distribution of hyperiidAmphipoda in theGulf of California. PhD thesis, University ofArizona

Stephensen K (1923) Crustacea Malacostraca. V. Amphipoda. I. DanIngolf Exped 3(8):1–100

Steuer A (1911) Adriatische Planktonamphipoden. Sitz KaiserlichenAkad Wiss, Math Natur Kl Wien 120:671–688, pls 1–3

Takahashi K, Ichikawa T, Saito H, Kakehi S, Sugimoto Y, Hidaka K,Hamasaki K (2013) Sapphirinid copepods as predators of doliolids:their role in doliolid mortality and sinking flux. Limnol Oceanogr58:1972–1984

Trégouboff G, Rose M (1957) Manuel de PlanctonologieMéditerranéene. Centre national de la Recherche Scientifique,Paris 1:1–587; 2: pls 1–207

Trasviña A, Lluch-Cota D, Filonov AE, Gallegos A (1999) Oceanografíay El Niño. In: Magaña V (ed) Los impactos del Niño en México.Cap 3, UNAM, Mexico, p 69–101

Turpaeva EP, Raiskii AK (2014) Deep-sea fauna of European seas: anannotated species check-list of benthic invertebrates living deeperthan 2000 m in the seas bordering Europe. Pycnogonida. Inv Zool11:240–247

Vinogradov ME, Volkov AF, Semenova TN (1996) Hyperiid amphipods(Amphipoda, Hyperiidea) of the world oceans. Science, Lebanon

Wiebe PH, Benfield MC (2003) From the Hensen net toward four-dimensional biological oceanography. Prog Oceanogr 56:7–136

Zeidler W (2012) A review of the hyperiidean amphipod familiesMimonectidae and Proscinidae (Crustacea: Amphipoda:Hyperiidea: Scinoidea). Zootaxa 3533:1–74

Mar Biodiv