floating nurseries? scyphozoan jellyfish, their food and their rich … · 2018-06-19 ·...

Submitted 8 February 2018Accepted 3 June 2018Published 19 June 2018

Corresponding authorJoseacute M Riascosjosemriascoscorreounivalleeduco

Academic editorAlex Ford

Additional Information andDeclarations can be found onpage 15

DOI 107717peerj5057

Copyright2018 Riascos et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Floating nurseries Scyphozoan jellyfishtheir food and their rich symbiotic faunain a tropical estuaryJoseacute M Riascos1 Willington Aguirre2 Charlotte Hopfe3 Diego Morales1Aacutengela Navarrete1 and Joseacute Tavera1

1 Instituto de Ciencias del Mar y Limnologiacutea Universidad del Valle Cali Colombia2Bahiacutea Maacutelaga Consejo Comunitario Comunidad Negra de La Plata Bahiacutea Maacutelaga Buenaventura Colombia3Department of Biomaterials Universitaumlt Bayreuth Bayreuth Germany

ABSTRACTBackground The anthropogenic modification of trophic pathways is seeminglyprompting the increase of jellyfish populations at the expense of planktivorous fishesHowever gross generalizations are oftenmade because themost basic aspects of trophicecology and the diverse interactions of jellyfish with fishes remain poorly describedHere we inquire on the dynamics of food consumption of the medusoid stage of thescyphozoan jellyfish Stomolophus meleagris and characterize the traits and diversity ofits symbiotic communityMethods S meleagris and their associated fauna were sampled in surface watersbetween November 2015 and April 2017 in Maacutelaga Bay an estuarine system at theColombian Pacific Stomach contents of medusae were examined and changes in preycomposition and abundance over time analysed using a multivariate approach Theassociated fauna was identified and the relationship between the size of medusae andthe size those organisms tested using least-square fitting proceduresResults The presence of S meleagris medusa in surface waters was seasonal The gutcontents analysis revealed that algae copepods and fish early life stages were the moreabundant items and PERMANOVA analysis showed that the diet differed within theseasons (P(perm) = 0001) but not between seasons (P(perm) = 0134) The majority ofthe collectedmedusae (504) were associated with individuals of 11 symbiotic species953of them fishes 31 crustaceans and 16molluscs Therefore this study reports10 previously unknown associations The bell diameter of S meleagris was positivelyrelated to the body sizes of their symbionts However a stronger fit was observed whenthe size relationship between S meleagris and the fishHemicaranx zeloteswasmodelledDiscussion The occurrence of S meleagris was highly seasonal and the observedpatterns of mean body size through the seasons suggested the arrival of adult medusaeto the estuary from adjacent waters The diet of S meleagris in the study area showeddifferences with previous reports chiefly because of the abundance of algae that areseemingly ingested but not digested The low number of zooplanktonic items in gutcontents suggest the contribution of alternative food sources not easily identifiableThe observed changes in the composition of food in the guts probably reflect seasonalchanges in the availability of prey items The regular pattern in the distribution ofsymbionts amongmedusae (a single symbiont per host) and the positive host-symbiontsize relationship reflects antagonistic intraspecific and interspecific behaviour of thesymbiont This strongly suggest that medusa represent an lsquolsquoeconomically defendable

How to cite this article Riascos et al (2018) Floating nurseries Scyphozoan jellyfish their food and their rich symbiotic fauna in a tropi-cal estuary PeerJ 6e5057 DOI 107717peerj5057

resourcersquorsquo that potentially increases the survival and recruitment of the symbionts tothe adult population We argue that if this outcome of the symbiotic association canbe proven scyphozoan jellyfish can be regarded as floating nurseries

Subjects Biodiversity Ecology Marine Biology Population BiologyKeywords Jellyfish blooms Feeding ecology Fisheries Scyphozoans Gelatinous zooplanktonFish recruitment Symbiosis Diversity of interactions Trophic ecology Estuaries

INTRODUCTIONThe magnitude and frequency of population blooms of jellyfish (pelagic cnidarian andctenophores) are seemingly increasing along with strong impacts on marine ecosystemsThe collapse of formerly rich fisheries has been linked to increasing jellyfish populationsin several regions (Lynam et al 2006 Brodeur Ruzicka amp Steele 2011) However much ofthe societal and even scientific perception about jellyfish and their role in ecosystems isbased on speculation limited evidence and flawed scientific practices (eg Haddock 2008Richardson et al 2009 Sanz-Martiacuten et al 2016) Trophic interactions between jellyfish andplanktivorous fishes have been characterized as a combination of mutual predation andcompetition for planktonic food (Purcell amp Arai 2001 Lynam et al 2006 Brodeur et al2008 Richardson et al 2009) Changes in the balance of these trophic pathways in stressedand overfished ecosystems have been hypothesized to explain massive local proliferationsof jellyfish that displace planktivorous fishes and form alternate jellyfish-dominatedecosystems (Richardson et al 2009) However trophic relationships are only known for asmall portion of this polyphyletic assemblage spanning more than 2000 species (Fleming etal 2015) As a result trophic models assessing food web structure and energy flow oftenignore jellyfish or include them as a single functional group with the characteristics of anlsquoaveragersquo jellyfish whose parameterization frequently varies greatly among models (Paulyet al 2009) In fact the hypotheses proposed to explain changes in jellyfish dominatedecosystems remain untested partially because there is a recognition thatmore basic researchon feeding ecology is still required (Pauly et al 2009 Richardson et al 2009 Naman et al2016)

Regarding scyphozoan jellyfish two emerging issues are challenging the predominantview of competitive trophic interactions between planktivorous fishes and jellyfish Firstrecent methodological approaches have shown that scyphozoans use unsuspected foodsources including benthic organisms (Pitt et al 2008 Ceh et al 2015) microplanktonand resuspended organic matter (Javidpour et al 2016) These food sources have beentraditionally overlooked because most studies on feeding ecology use gut content analysisthat focuses on mesozooplankton and ichthyoplankton presumably because they aremore visible and retained in the gut for longer than other type of food (Pitt Connolly ampMeziane 2009) Thus the widely held view that fishes and scyphozoan jellyfish competefor the same food source seems a gross generalization Second mounting evidence suggeststhat mutual predation (ie medusae predating on fish egg or larvae and fishes predatingon medusae early life stages) is only one side of the story Scyphozoans usually display

Riascos et al (2018) PeerJ DOI 107717peerj5057 222

lsquolsquosymbiotic associationsrsquorsquo defined as any living arrangement including positive andnegative associations between members of two different species (see Martin amp Schwab2013) Symbionts are diverse ranging from fish to invertebrates in a variety of relationshipsincluding parasitism mutualism and commensalism (Riascos et al 2013 Ohtsuka et al2009 Ingram Pitt amp Barnes 2017) However trophic modelling efforts traditionally focuson predation and competition despite mounting evidence showing that alternative trophicpathways and relationships may positively affect fish populations (eg Lynam amp Brierley2007 Riascos et al 2012 Greer et al 2017)

Much of the prevalent view about fish-jellyfish trophic dynamics is derived fromscyphozoans of subtropical and temperate areas that support large pelagic fisheries Inestuarine systems the scarce evidence suggests a low trophic overlap between fish andjellyfish (Nagata et al 2015 Naman et al 2016) and a high occurrence of symbioticassociations with juveniles of fish and invertebrates (eg Rountree 1983 Costa Albieriamp Arauacutejo 2005 Martinelli et al 2008) perhaps reflecting the abundance of early stagesof coastal fauna in nursery areas Hence there is a need to study the trophic ecologyof scyphozoan jellyfish and their multiple biological interactions to truly understandpopulation dynamics their position in food webs and their functional role in estuarineecosystems

Here we studied the canonball jellyfish Stomolophus meleagris (Agassiz 1862) in theestuarine ecosystem of Malaga Bay an area of high biodiversity in the Colombian pacificcoast This species is widely distributed in the western Atlantic (United States to Brazil)and the Pacific oceans (southern California to Ecuador Sea of Japan to South China Sea)(Calder 1982 Griffin amp Murphy 2011) and has been described as a specialized predator offish eggs copepods and mollusc larvae with the capacity to regulate local populations ofits prey (Larson 1991) Therefore the aims of this study were (i) to assess changes in thestructure of the diet in the study area and (ii) analyse the traits diversity and significanceof the symbiotic associations in the estuarine ecosystem

MATERIALS amp METHODSSamplingThe study was performed in Maacutelaga Bay a south-facing bay located in the central regionof the Colombian Pacific coast (405primeN and 7716primeW Fig 1) The bay is located withinthe Chocoacute-Darien region an area with one of the highest levels of precipitation in thewestern hemisphere (7000ndash11000 mm Poveda Jaramillo amp Vallejo 2014) which has twowet seasons during the year AprilndashJune and SeptemberndashNovember The water depth inthis bay averages 13 m but reaches a maximum of 40 m Tides are semi-diurnal with amean tidal range of 41 m Sea surface temperature varies between 25 and 30 C and salinitybetween 19 and 28 in the mouth of the bay and 13 and 10 close to small rivers (Lazarusamp Cantera 2007) Sampling of S meleagris was conducted around La Plata Archipielagoat the innermost part of Maacutelaga Bay Samplings were allowed by the Autoridad Nacionalde Licencias Ambientales (ANLA permit number 1070_28-08-2015) The medusoid phaseshowed a seasonal occurrence in surface waters December 2015 to May 2016 (hereafterseason 1) and December 2016 to April 2017 (hereafter season 2) Sampling effort was


Figure 1 Map of the study area in La Plata Archipelago (Maacutelaga Bay Colombian Pacific coast)Full-size DOI 107717peerj5057fig-1


relatively constant throughout the seasons when medusae were detected three or fourthree-hour sighting trips were performed per month Medusae were sampled from a smallboat using dip nets and the relative abundance was estimated as the number of caughtmedusae per hour As medusas where generally associated to juvenile fish or invertebratesthe sampling was limited to 15 to 20 medusae per month to avoid disturbing populationsof fish potentially under conservation Upon collection medusae discharged a stickymucusthat rapidly killed fish or associated invertebrates as reported by Shanks amp Graham (1988)Thereafter medusae and their associated fauna were tagged and stored in individual jarswith 5 borate buffered formaldehyde solution in seawater

In the laboratory the bell diameter of each medusa and the standard length of associatedfish and invertebrates (crustaceans and molluscs) were measured using callipers Themedusarsquos fused oral arms and the mouth folds were excised and rinsed through a 100-micrommesh sieve to concentrate food particles The resulting material was transferred to ethanoland sorted for the presence of prey items using a dissecting microscope Prey itemswere determined to a taxonomic level suitable for making meaningful comparisons withsimilar studies (Larson 1991 Padilla-Serrato et al 2013 Aacutelvarez Tello Loacutepez-Martiacutenez ampLluch-Cota 2016)

Associated fish were identified to species according to current keys and by comparison oftheirmorphological features against available descriptions (Jordan amp Evermann 1898Allenamp Robertson 1994 Fischer et al 1995 Chirichigno amp Cornejo 2001 Robertson amp Allen2015) Molluscs and crustaceans were identified by Cantera JR and JF Lazarus respectivelyFinally all the associated fauna was stored as reference material in the scientific collectionat the Marine Biology section at Universidad del Valle

Data analysesA multivariate approach was used to test changes in the structure (composition andabundance) of the diet over time For this data were arranged in a matrix of abundance ofeach taxon (rows) eaten by individual medusae in each month (columns) Prey taxa withfew occurrences (lt01 of total abundance Table 1) were excluded from further analysesPrior to the analyses data were standardized to account for the difference in food quantityassociated to distinct medusae body sizes by dividing the abundance of each prey item bythe total abundance of prey for each medusa Moreover data were square root transformedto slightly downweigh the contribution of abundant food items

Non-metric multidimensional scaling (nMDS Clarke amp Gorley 2006) was used to buildan ordination plot of medusae per month and season calculated from a BrayndashCurtis matrixof similarity in diet composition The distance-based permutational multivariate analysisof variance (PERMANOVA Anderson 2001) was used to test for temporal differencesin the structure of diet between months and seasons The model used lsquolsquomonthrsquorsquo as arandom factor nested within the fixed factor lsquolsquoseasonrsquorsquo As the PERMANOVA approach issensitive to differences in multivariate dispersion within groups the PERMDISP routinewas used to test for homogeneity of dispersions Thereby a preliminary analysis showedthat multivariate dispersion was strongly dependent of sample size with less dispersionobserved at the beginning of the season when medusae were scarce in the field and thus


Table 1 Composition andmean abundance (number of food item per medusa and standard error in brackets) of food items in gut contents of Stomolophus melea-gris during two seasons in Bahiacutea Maacutelaga Pacific coast of Colombia

Season 1 (2015ndash2016) Season 2 (2017) Rel

Food iacutetem Dec Jan Feb Mar Apr May Jan Feb Mar Apr Tot Ab ()

Bacillariophyta Coscinodiscophyceae 0 (0) 15 (21) 62 (94) 121 (30) 96 (132) 19 (49) 16 (19) 06 (07) 02 (05) 17 (39) 561 181

Crustacea Copepoda adult 375 (148) 4 (57) 55 (48) 32 (31) 61 (138) 18 (19) 24 (38) 09 (15) 07 (1) 34 (52) 444 143

Bacillariophyta Bacillariophyceae 05 (07) 145 (78) 78 (156) 17 (52) 37 (6) 29 (59) 16 (17) 16 (25) 13 (2) 54 (81) 395 128

Chordata Fish (eggs amp larvae) 1 (0) 6 (14) 31 (38) 36 (41) 32 (62) 39 (106) 06 (13) 19 (25) 07 (13) 21 (27) 308 99

Crustacea Unidentified 0 (0) 0 (0) 09 (33) 07 (23) 27 (41) 18 (22) 16 (15) 18 (32) 43 (32) 54 (37) 286 92

Mollusca Bivalve larvae 0 (0) 2 (28) 22 (28) 37 (5) 19 (43) 08 (14) 1 (1) 25 (25) 06 (08) 28 (33) 229 74

Mollusca Gastropod larvae 0 (0) 65 (92) 34 (47) 19 (37) 14 (23) 07 (15) 0 (0) 32 (34) 05 (14) 02 (04) 193 62

Crustacea Cirripedia larvae 1 (0) 0 (0) 08 (13) 05 (11) 15 (24) 0 (0) 06 (05) 13 (19) 03 (08) 03 (07) 88 28

Chaetognatha Sagittoidea 1 (14) 0 (0) 02 (08) 07 (13) 13 (21) 05 (12) 26 (24) 04 (09) 0 (02) 03 (07) 75 24

Ciliophora 0 (0) 0 (0) 0 (0) 0 (0) 06 (16) 0 (0) 64 (143) 0 (0) 0 (0) 0 (0) 46 15

Annelida Polychaeta larvaejuvenile 0 (0) 0 (0) 01 (03) 03 (1) 01 (03) 02 (08) 04 (05) 03 (07) 04 (08) 03 (07) 31 10

Crustacea Brachiura larvae 0 (0) 1 (14) 05 (09) 01 (03) 02 (07) 02 (06) 0 (0) 03 (04) 01 (03) 01 (03) 25 08

Nematoda 0 (0) 0 (0) 0 (0) 01 (05) 0 (02) 03 (06) 02 (04) 04 (07) 02 (05) 0 (0) 19 06

Crustacea Amphipoda adult 1 (14) 0 (0) 0 (0) 0 (0) 0 (02) 0 (0) 02 (04) 0 (0) 0 (02) 03 (1) 8 03

Crustacea Anomura (Emerita sp) adult 0 (0) 0 (0) 0 (0) 0 (0) 02 (05) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 4 01

Unidentified 55 (21) 115 (64) 45 (46) 43 (4) 22 (34) 32 (48) 48 (38) 3 (29) 25 (31) 06 (09) 386 125

Average number of prey items 475 (93) 47 (45) 352 (26) 328 (31) 347 (26) 183 (13) 24 (18) 182 (11) 12 (11) 231 (19) 293

Riascos

etal(2018)PeerJDOI107717peerj5057

622

0

20

40

60

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100

120

140

0

5

10

15

20

25

30

D J 2016 F M A M

Mean b

ell

dia

mete

r (m

m)

+S

D

Rela

tive a

bundance (

ind h

-1)

A

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20

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D J 2017 F M A M

Mean b

ell

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-1)

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Figure 2 Monthly variability of bell diameter and relative abundance of Stomolophus meleagris in LaPlata Archipelago (Maacutelaga Bay Colombia) during twomedusoid seasons Grey bars represent bell di-ameter and black lines the relative abundance of Stomolophus meleagris Seasons are December 2015ndashMay 2016 (A) December 2016ndashMay 2017 (B)

Full-size DOI 107717peerj5057fig-2

sample size was smaller Therefore samples from December 2015 (N = 2) January 2015(N = 2) and January 2016 (N = 5) were excluded from the analysis Finally when temporaldifferences were confirmed by the PERMANOVA a Canonical Ordination of PrincipalCoordinates (CAP Anderson amp Willis 2003) was used as a constrained ordination that bestdefines groups (months) according to the diet structure

To assess if the body sizes of medusae and their symbionts are related length datawere fitted to linear polynomial logarithmic exponential and power models The bestfit was chosen according to the proportion of variance explained Models were fitted byleast squares procedures using the algorithm LevenbergndashMarquardt to estimate standarderrors (SE) of the parameters Finally we performed a literature review of the reportedsymbiotic fauna for S meleagris to compare the diversity of associations found in thestudy area The terms lsquolsquoStomolophusrsquorsquo and lsquolsquoStomolophus meleagrisrsquorsquo excluding the termslsquolsquovenomrsquorsquo lsquolsquoproteinrsquorsquo and proteomicsrsquorsquo from the title or in combination with lsquolsquoassociationrsquorsquolsquolsquosymbiosisrsquorsquo or lsquolsquorelationshiprsquorsquo were used to search the ISI Web of Science database andGoogle Scholar The resulting literature was then manually scanned for descriptions ofsymbiotic relationships

RESULTSJellyfish seasonalityTwo species of scyphozoan jellyfish were found during this study S meleagris and Pelagianoctiluca The latter was found only occasionally one individual during season 1 and sixduring the season 2 Such a small sample size circumvents any quantitative analysis andtherefore only descriptive details will be given The relative abundance of S meleagrisconsistently showed a unimodal pattern with peaks during March or April (Fig 2)Moreover the bell diameter did not show a consistent pattern of growing or decreasing sizeover time


2D Stress 026

Dec

Jan

Feb

Mar

Apr

May

Season 1

Jan

Feb

Mar

Apr

Season 2

Figure 3 nMDS ordination plot on the diet composition of Stomolophus meleagris nMDS calculatedfrom BrayndashCurtis dissimilarity measures with square-root transformed data of abundance per food itemduring two medusoid seasons (December 2015ndashMay 2016 and Jan 2017ndashApr 2017)


The dynamics of food consumption by S meleagrisThe composition and abundance of food items consumed by S meleagris is shown inTable 1 The diet was prevalently comprised of bacillariophyte algae copepods and fishearly stages Small amounts of benthic items (eg juvenile polychaetes amphipods andadult Emerita sp) were found frequently and suggest that S meleagris feeds near thebottom A few nematods typically jellyfish parasites were also found but included as fooditems because they were not buried in the hostrsquos tissue as observed by Phillips amp Levin(1973) and showed obvious signs of digestion Arguable between-month differences in dietcomposition were apparent form the nMDS ordination (Fig 3) particularly when the samemonth from different seasons were compared (eg March in each season) However as thePERMDISP test was significant for the factor lsquolsquomonthrsquorsquo (F9111= 4242 P(perm)= 0006)a PERMANOVA might yield misleading results To circumvent this problem monthswith small sample sizes (N le 5) were excluded (PERMDISP test not significant monthF6105= 2183 P(perm)= 0066 season F1110= 1ndash734 P(perm)= 0211)

The PERMANOVA analysis (Table 2A) showed significant differences in the structureof the diet of S meleagris among months (P(perm) = 0001) but not between seasons(P(perm)= 0134) Pair-wise comparisons (Table 2B) revealed between-month differenceswhich were best illustrated by the CAP constrained ordination (Fig 4) Scyphozoan jellyfishare widely considered carnivore predators and as such the inclusion of phytoplanktonitems in the analysis of diet composition seems unwarranted and the described dynamicsof food consumption questionable Therefore the PERMANOVA analysis was re-runwith exclusion of the Coscinodiscophyceae and Bacillariophyceae This analysis rendered


Table 2 Results of (A) the PERMANOVA analysis on the differences in the structure of the diet of Sto-molophus meleagris amongmonths and seasons and (B) pair-wise tests for differences between pairs ofmonths in each season

A Source df SS MS Pseudo-F P (perm) Unique perms

Season 1 10841 10841 22673 0134 917Month(season) 5 24981 4996 24719 0001 998Res 105 212230 2021Total 111 249810

B Months Season T P (perm) perms

February March 1 1440 0077 999February April 1 1427 0087 999February May 1 1395 0083 998March April 1 1717 0017 999March May 1 1510 0041 999April May 1 0982 0486 997February March 2 2101 0004 999February April 2 1830 0016 998March April 2 1270 0151 999

NotesSignificant factors (α= 005) are highlighted in bold

remarkably similar results significant differences in the structure of the diet amongmonths(P(perm)= 0002) but not between seasons (P(perm)= 0128) (Table S1)

Traits and diversity of the biological associationsThe body size of the 121 collected S meleagris ranged between 121 and 1092 mm inbell diameter The prevalence of symbiotic associations (ie the percentage of medusaharbouring symbionts) was high with 504 of the collected specimens With only threeexceptions a single symbiont per medusa was found clearly indicating that the distributionof symbionts among host was not random but uniform The symbiotic community ofS meleagris was composed of fishes (953) crustaceans (31) and molluscs (16)(Fig 5) Generally associated fish reacted to disturbance by hiding within oral arms orbelow the hostrsquos bell it could be said that fish lsquolsquoresist efforts to separate themrsquorsquo as statedby Hargitt (1904) However the prevalence of symbiotic association might have beenunderestimated because some may have escaped during the sampling Regularly only onesymbiont per host was found with only three exceptions where two fish per medusa whereobserved P noctiluca also had symbiotic associations two out of six medusae harbouredindividual fish (Hemicaranx zelotes)

The body size of the scyphozoan S meleagris showed a significant positive correlationwith the body size of its symbiotic community as a whole the fish assemblage andH zelotesin particular (Fig 5 Table 3) Power models best fitted the positive body size relationshipsand the model including only H zelotes had the highest proportion of variability explained(0634) This partially reflects the fact that H zelotes was the most common symbiontof S meleagris Figure 5 shows that the symbionts were generally smaller than the host


-010 -005 0 005 010 015

CAP1

-010

-005

0

005

010

015

C A

P 2

Feb

Mar

Apr

Season 2

Feb

Mar

Apr

May

Season 1

Figure 4 Constrained Canonical Analysis of Principal Coordinates of the diet composition of Sto-molophus meleagris CAP analysis based in BrayndashCurtis dissimilarity measures with square-root trans-formed data of abundance per food item during two medusoid seasons (December 2015ndashMay 2016 andJan 2017ndashApr 2017)


However less frequent symbionts did not follow that pattern for instance Centropomusmedius Lutjanus guttatus Oligoplites altus Selene brevoortii and Gerres similimus werelarger and Hyporhamphus snyderi almost twice as large as its host

The richness of the symbiotic fauna reported for S meleagris in the study area wasunexpectedly high 11 species 10 of them being new reports of symbionts for this speciesThis richness represents 392 of the total diversity of associations found so far (28symbiotic species reported Table 4) for this widely-distributed scyphozoan jellyfish

DISCUSSIONThe occurrence of S meleagris in the study area showed a consistent seasonal pattern thatcoincides with the seasonal increase in the sea surface temperature from January to May inthe study area (IDEAM 2004) The body size did not show an increasing trend through theseasons This suggest that the observed medusae did not recruit from local benthic polypsbut arrive to the estuarine system as adults from adjacent areas as discussed by Kraeuter ampSeltzler (1975) for S meleagris in Georgian and North Carolina waters

There are only three published studies on feeding ecology of S meleagris Taken togetherthese studies highlight that a few taxa form a high percentage of the total gut contentLarson (1991) found that in the north-eastern Gulf of Mexico 98 of S meleagris diet


0

20

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160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)

Stomolophus meleagris body size (mm)

Hemicaranx zelotes

Hyporhamphus snyderi

Centropomus medius Lutjanus guttatus Oligoplites altus Selene brevoortii Gerres similimus Atherinella argentea Chloroscombrus orqueta Lolingula panamensis Penaeus stylirrostris

Figure 5 Body size relationships between Stomolophus meleagris and its symbiotic fauna Lines rep-resent the model fits for Hemicaranx zelotes fishes and the whole symbiotic community Parameter esti-mations and associated statistics for each model are given in Table 3 The dotted lined circle represents aH zelotes excluded from the analysis as its association to the respective medusa could not be confirmedwith certainty


Table 3 Results of the model fitting procedure on the relationship of the body size of Stomolophus me-leagris and its symbionts

Associates Model a (SE) b (SE) Pr Var F -value p

Fish Y = aXb 1551 (1202) 0809 (0189) 0291 134763 lt0001All Y = aXb 1775 (1371) 0775 (0189) 0269 138378 lt0001H zelotes Y = aXb 1204 (0486) 0830 (0098) 0634 412441 lt0001

NotesPrVar Proportion of variability explained by the model

was composed of bivalve veligers tintinnids copepods gastropod veligers and Oikopleura(Appendicularia) In the Gulf of California off the coast of Sonora gut contents weredominated by fish eggs (ca 83 in a study by Padilla-Serrato et al 2013 and ca 59in a study by Aacutelvarez Tello Loacutepez-Martiacutenez amp Lluch-Cota 2016) followed by mollusclarvae (sim26) and copepods (sim11) (Aacutelvarez Tello Loacutepez-Martiacutenez amp Lluch-Cota 2016)Although our results (Table 1) also show that a few items comprise high percentages of thediet the composition and relative importance of those items varied strongly among studiessuggesting strong spatialndashtemporal differences in food composition The main differencewith previous studies is the consistency of Bacillariophyta among ingested items surprisingfor a scyphozoan considered carnivore However the fact that phytoplankton items did not


Table 4 List of published (a) and new (b) reports on symbionts of the cannonball jellyfish Stomolophus meleagris An unidentified cestode larvawas reported by Phillips amp Levin (1973) though it is not included in the list

Class family Species Locality and literature source

(a)Actinopterygii Carangidae Chloroscombrus chrysurus (Linnaeus 1766) Mississippi Sound Mississippi USA (Phillips Burke amp

Keener 1969)Wrightsville Beach North Carolina USA (Rountree 1983)Onslow Bay North Carolina USA (Shanks amp Graham1988)Texas USA (Baughman 1950)

Hemicaranx amblyrhynchus (Cuvier 1833) Western Golf of Mexico USA amp Mexico (Hildebrand 1954)Hemicaranx zelotes Gilbert 1898 Kino Bay Sonora Mexico (Loacutepez amp Rodriacuteguez 2008)

Maacutelaga Bay Pacific coast Colombia (This study)Caranx crysos (Mitchill 1815) Barataria Bay Louisiana USA (Gunter 1935)Caranx hippos (Linnaeus 1766) Wrightsville Beach North Carolina USA (Rountree 1983)Carangoides bartholomaei (Cuvier 1833) Wrightsville Beach North Carolina USA (Rountree 1983)

Actinopterygii Stromateidae Peprilus triacanthus (Peck 1804) Wrightsville Beach North Carolina USA (Rountree 1983)Beaufort North Carolina USA (Smith 1907)Port Aransas Texas USA (Hoese Copeland amp Miller 1964)Western Golf of Mexico USA amp Mexico (Hildebrand 1954)Gulf of Mexico USA (Horn 1970)

Peprilus burti Fowler 1944 Gulf of Mexico USA (Horn 1970)Peprilus paru (Linnaeus 1758) Mississippi Sound Mississippi USA (Phillips Burke amp

Keener 1969)Port Aransas Texas USA (Hoese Copeland amp Miller 1964)

Actinopterygii Monacanthidae Stephanolepis hispida (Linnaeus 1766) Mississippi Sound Mississippi USA (Phillips Burke ampKeener 1969)Wrightsville Beach North Carolina USA (Rountree 1983)Onslow Bay North Carolina USA (Shanks amp Graham1988)

Aluterus schoepfii (Walbaum 1792) Wrightsville Beach North Carolina USA (Rountree 1983)Woods Hole Massachusetts USA (Hargitt 1904)

Actinopterygii Nomeidae Nomeus gronovii (Gmelin 1789) Beaufort North Carolina USA (Smith 1907)Japan amp Hong Kong (Morton 1989)

Malacostraca Epialtidae Libinia dubiaH Milne Edwards 1834 Beaufort North Carolina USA (Gutsell 1928)Mississippi Sound Mississippi USA (Phillips Burke ampKeener 1969)South Carolina USA (Corrington 1927)Wrightsville Beach North Carolina USA (Rountree 1983)Onslow Bay North Carolina USA (Shanks amp Graham1988)Fort Pierce Florida USA (Tunberg amp Reed 2004)

Libinia sp Texas coast USA (Whitten Rosene amp Hedgepeth 1950)Libinia emarginata Leach 1815 Western Golf of Mexico USA amp Mexico (Hildebrand 1954)

(continued on next page)


Table 4 (continued)


Malacostraca Portunidae Charybdis (Charybdis) feriata (Linnaeus 1758) Japan amp Hong Kong (Morton 1989)Hexanauplia Lepadidae Conchoderma virgatum Spengler 1789 Guaymas Mexico (Aacutelvarez Tello Loacutepez-Martiacutenez amp

Rodriacuteguez-Romero 2013)Cestoda Otobothriidae Otobothrium dinoi (Mendez 1944) Palm 2004 Cananeacuteia Sao Paulo Brazil (Vannucci 1954)(b)Actinopterygii Carangidae Chloroscombrus orqueta Jordan amp Gilbert 1883 Maacutelaga Bay Pacific coast Colombia

Oligoplites altus (Gunther 1868) Maacutelaga Bay Pacific coast ColombiaSelene brevoortii (Gill 1863) Maacutelaga Bay Pacific coast Colombia

Actinopterygii Atherinopsidae Atherinella argentea Chernoff 1986 Maacutelaga Bay Pacific coast ColombiaActinopterygii Gerreidae Gerres simillimus Regan 1907 Maacutelaga Bay Pacific coast ColombiaActinopterygii Centropomidae Centropomus medius Guumlnther 1864 Maacutelaga Bay Pacific coast ColombiaActinopterygii Hemiramphidae Hyporhamphus snyderi Meek amp Hildebrand 1923 Maacutelaga Bay Pacific coast ColombiaActinopterygii Lutjanidae Lutjanus guttatus (Steindachner 1869) Maacutelaga Bay Pacific coast ColombiaMalacostraca Penaeidae Penaeus stylirostris Stimpson 1871 Maacutelaga Bay Pacific coast ColombiaCephalopoda Loliginidae Lolliguncula (Lolliguncula) panamensis

Berry 1911Maacutelaga Bay Pacific coast Colombia

influence the temporal patterns in the structure of gut contents suggest a level of structuralredundancy (ie many items are interchangeable in the way they define changes incomposition through time sensu Clarke amp Warwick 1998) However finding an ingesteditem does not mean that it is digested which is one general limitation of studying feedingpatterns of jellyfish by gut contents (Pitt Connolly amp Meziane 2009) As Bacillariophyceae(Nitzschia) and Coscinodiscophyceae (Coscinodiscus Rhizosolenia) are among the mostabundant phytoplankton components in Maacutelaga Bay (Prahl Cantera amp Contreras 1990) itseems reasonable to apply Ockham rsquos principle and assume that the presence of algae in gutcontents only reflect their abundance in the water column Interestingly Larson (1991) alsostates that lsquolsquoCoscinodiscus sp was abundant in gut contentsrsquorsquo but it was not listed as preytaxa It is worth noting that the assumption that jellyfish feed on mesozooplankton andichthyoplankton is probably related with the essentially arbitrary use of 60ndash100 microm sievesto concentrate the samples for gut content analysis In fact when alternative methods likegrazing experiments microvideographic techniques stable isotopes and fatty acid tracersare used it becomes apparent that jellyfish can also feed on microzooplankton (Sullivan ampGifford 2004 Colin et al 2005) demersal zooplankton (Pitt et al 2008) and resuspendedorganicmatter (Javidpour et al 2016) Therefore our results should be regarded as a partialdepiction of the diet composition of S meleagris

As body size of S meleagris did not show a consistent pattern of growth over time (Fig 2)the intra-season variability observed in the structure of the diet could not be attributedto ontogenetic changes in food habits In fact the diet composition of the smaller andlarger medusae observed in December 2015 and January 2016 respectively (Fig 2) wasvery similar (Fig 3) Therefore the observed intra-season variability might be related withchanges in the availability of prey in the water column but information to evaluate thishypothesis is lacking


The lack of significant differences in the diet structure of S meleagris between seasonswas surprising because the first medusoid season coincided with the major El Nintildeo-La Nintildeacycle 2015ndash2016 which heavily modified temperature and rainfall patterns in the studyarea (Riascos Cantera amp Blanco-Libreros 2018) For example it is known that the strongmodification of freshwater nutrient subsidies through precipitation in Maacutelaga Bay driveschanges in the population dynamics and reproductive cycle of benthic estuarine bivalves(Riascos 2006 Riascos Heilmayer amp Laudien 2008) Hence it would be reasonable toexpect shifts in the abundance and composition of the zooplankton community associatedto El Nintildeo-La Nintildea 2015ndash2016 during the first season which would be then reflected insignificant changes in the diet structure of S meleagris between seasons It is difficult tospeculate on reasons for this result but perhaps El Nintildeo-La Nintildea modified the compositionof the zooplankton community at lower taxonomic levels (eg species families) whichwe were not able to detect owed to our categorization of prey items at higher taxonomiclevels (Table 1)

Marshes mangrove forests and seagrass meadows have long been recognized as nurserygrounds mainly because they have extremely high primary and secondary productivity andsupport a great abundance and diversity of early life stages of fish and invertebrates (Beck etal 2001) Recently Doyle et al (2014) analysed the role of jellyfish as lsquolsquoservice providersrsquorsquoin pelagic habitats and described jellyfish as habitat and nurseries because they are (i)larger than most planktonic organisms (ii) slower swimmers than most nektonic animalsand (iii) their diverse morphology provide three-dimensional space for refuge or shelterClearly those facts alone do not meet the premise that lsquolsquoa habitat is a nursery for juvenilesof a particular species if its contribution per unit area to the production of individuals thatrecruit to adult populations is greater on average than production from other habitats inwhich juveniles occurrsquorsquo (Beck et al 2001) Strictly speaking this is a hypothesis remainingto be tested though some of our results suggest that S meleagris occurring in estuarinesystems provide a valuable resource that may significantly increase the survivorship andrecruitment of juvenile fishes or invertebrates First the great dominance of H zelotesamong a diversity of other symbionts suggest a higher suitability to its host This is in linewith the fact that fish of the family Carangidae are the most commonly reported symbiontof S meleagris (Table 4) Secondly the high prevalence of an association and a uniformdistribution of the symbiont within the host population as those observed for H zelotesand S meleagris strongly suggest intraspecific and interspecific interactions and territorialbehaviour (Connell 1963 Britayev et al 2007 Riascos et al 2011) And thirdly positivesymbiont-host size relationships as those observed when H zelotes the fish assemblageand the whole symbiotic assemblage are analysed suggest either parallel growth of thehost and the symbiont (Britayev amp Fahrutdinov 1994) or size-segregation behaviour by thesymbiont (Adams Edwards amp Emberton 1985 Hobbs amp Munday 2004)

Ecological theory predicts that competition and the lsquolsquoeconomic defendabilityrsquorsquo of aresource (sensu Brown 1964) facilitate or hinder the evolution of territoriality resourcesare monopolized whenever the benefits exceed the costs of defence Individuals of aterritorial species that fail to obtain a limited resource often make no contribution tofuture generations (Begon Harper amp Townsend 2006) For jellyfish-fish associations there


is correlational data suggesting that the shelter andor food provided by jellyfish increasethe survival of juvenile fish to adulthood (Lynam amp Brierley 2007) In this context if theseasonal occurrence of S meleagris does represent a defendable resource and the influenceon the survival of its symbiotic fauna could be experimentally demonstrated this speciesmay be considered a floating nursery

According to Castro Santiago amp Santana-Ortega (2002) 333 species of fish belongingto 96 families show aggregative or associative behaviour with floating algae gelatinouszooplankton whales flotsam or man-made fish aggregating devices and 14 of thesefamilies associate with jellyfish Therefore one may reasonably argue that if the jellyfish-fish association have a measurable effect on fish populations it can be considered marginalBut how complete is our knowledge of these associations Regarding S meleagris Table 4hints on this question First of all it shows that only a few areas of the species distributionrange have been studied particularly the western coast of United States and the Gulfof Mexico Second and more importantly the fact that the findings of our short-termstudy performed in a small tropical estuarine system represent ca 40 of the knowndiversity of the symbiotic fauna of S meleagris strongly suggest that diversity of symbiontsincrease toward tropical areas and that it is heavily underestimated Indeed the seven-yearmonitory of the bycatch in the trawl fishery of S meleagris off Georgia by Page (2015)rendered 38 species of finfish and three species of invertebrates Of course these cannot perse be assumed to be symbionts of S meleagris But the fact that three species known to becommon associates (Peprilus paru P triacanthus and Chloroscombrus chrysurus PhillipsBurke amp Keener 1969 Rountree 1983) comprised 63 of the bycatch strongly suggest thatsome of the other species may actually be unrecognised symbionts To conclude a moreprecise account of the diversity of symbiotic fish-jellyfish associations and an evaluation oftheir ecological significance may provide a more balanced view of the relationship betweenfish and jellyfish in marine ecosystems

ACKNOWLEDGEMENTSThanks to the lsquolsquoComunidad Negra de La Plata Bahiacutea Maacutelagarsquorsquo for their hospitality and forallowing access to their beautiful territory Thanks to Lazarus JF and Cantera JR for theirhelp in identifying crustaceans and molluscs respectively This is the publication number001 of the Instituto de Ciencias del Mar y Limnologiacutea (INCIMAR) Universidad del Valle

ADDITIONAL INFORMATION AND DECLARATIONS

FundingFunding for this research was provided by Universidad del Valle This research wassupported by a scholarship to Joseacute M Riascos by the Departamento Administrativo deCiencia Tecnologiacutea e Innovacioacuten (Colciencias) - Programa lsquolsquoTiempo de Volverrsquorsquo Thefunders had no role in study design data collection and analysis decision to publish orpreparation of the manuscript


Grant DisclosuresThe following grant information was disclosed by the authorsUniversidad del ValleDepartamento Administrativo de Ciencia Tecnologiacutea e Innovacioacuten (Colciencias)

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Joseacute M Riascos conceived and designed the experiments performed the experimentsanalyzed the data prepared figures andor tables authored or reviewed drafts of thepaper approved the final draftbull WillingtonAguirre conceived and designed the experiments performed the experimentsauthored or reviewed drafts of the paper approved the final draft contributed traditionalknowledge about local populations of jellyfish in the study areabull Charlotte Hopfe performed the experiments analyzed the data prepared figures andortables authored or reviewed drafts of the paper approved the final draftbull Diego Morales and Aacutengela Navarrete performed the experiments contributedreagentsmaterialsanalysis tools prepared figures andor tables authored or revieweddrafts of the paper approved the final draftbull Joseacute Tavera analyzed the data authored or reviewed drafts of the paper approved thefinal draft identified fish species

Animal EthicsThe following information was supplied relating to ethical approvals (ie approving bodyand any reference numbers)

During the course of the field work fish and a cephalopod associated with jellyfish wereincidentally caught Associated animals were deposited in the scientific collection of marinebiology at Universidad del Valle

Field Study PermissionsThe following information was supplied relating to field study approvals (ie approvingbody and any reference numbers)

Samplings were approved by the Autoridad Nacional de Licencias Ambientales (ANLApermit number 1070_28-08-2015)

Data AvailabilityThe following information was supplied regarding data availability

The raw data are provided in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj5057supplemental-information


REFERENCESAdams J Edwards AJ Emberton H 1985 Sexual size dimorphism and assortive mating

in the obligate coral commensal Trapezia ferruginea Latreille (Decapoda Xanthidae)Crustaceanea 48188ndash194 DOI 101163156854085X00882

Allen GR Robertson DR 1994 Fishes of the tropical Eastern Pacific Honolulu Univer-sity of Hawaii Press

Aacutelvarez Tello FJ Loacutepez-Martiacutenez J Lluch-Cota DB 2016 Trophic spectrum andfeeding pattern of cannonball jellyfish Stomolophus meleagris (Agassiz 1862) fromcentral Gulf of California Journal of the Marine Biological Association of the UnitedKingdom 96(6)1217ndash1227 DOI 101017S0025315415001605

Aacutelvarez Tello FJ Loacutepez-Martiacutenez J Rodriacuteguez-Romero J 2013 Primer registro dela asociacioacuten entre Stomolophus meleagris (Cnidaria Scyphozoa Rhizostomeae)y Conchoderma cf virgatum (Crustacea Cirripedia Thoracica) en el Golfo deCalifornia Hidrobiologica 23(1)138ndash142

AndersonMJ 2001 A new method for non-parametric multivariate analysis of varianceAustral Ecology 2632ndash46

AndersonMJWillis TJ 2003 Canonical analysis of principal coordinates a usefulmethod of constrained ordination for ecology Ecology 84(2)511ndash525DOI 1018900012-9658(2003)084[0511CAOPCA]20CO2

Baughman JL 1950 Random notes on Texas fishes Part II Texas Journal of Science2(2)242ndash263

BeckMW Heck Jr KL Able KW Childers DL Eggleston DB Gillanders BM HalpernB Hays CG Hoshino K Minello TJ Orth RJ Sheridan PFWeinsteinMP 2001The identification conservation and management of estuarine and marine nurseriesfor fish and invertebrates a better understanding of the habitats that serve asnurseries for marine species and the factors that create site-specific variability innursery quality will improve conservation and management of these areas Bioscience51(8)633ndash641 DOI 1016410006-3568(2001)051[0633TICAMO]20CO2

BegonM Harper JL Townsend CR 2006 Ecology from individuals to ecosystems fourthedition Oxford Blackwell Science

Britayev TA Fahrutdinov RR 1994 Pontoniin shrimps associated with molluscs at thecoast of South Vietnam (in Russian) In Pavlov DS Sbikin JN eds Hydrobionts ofSouth Vietnam Moscow Nauka 128ndash145

Britayev TA Martin D Krylova EM Von Cosel R Aksiuk TS 2007 Life-history traitsof the symbiotic scale-worm Branchipolynoe seepensis and its relationships withhost mussels of the genus Bathymodiolus from hydrothermal ventsMarine Ecology28(1)36ndash48 DOI 101111j1439-0485200700152x

Brodeur RD Ruzicka JJ Steele JH 2011 Investigating alternate trophic pathwaysthrough gelatinous zooplankton and planktivorous fishes in an upwelling ecosystemusing end-to-end models In Interdisciplinary studies on environmental chemistryndashmarine environmental modeling amp analysis Tokyo TERRAPUB 57ndash63


Brodeur RD Suchman CL Reese DC Miller TW Daly EA 2008 Spatial overlap andtrophic interactions between pelagic fish and large jellyfish in the northern CaliforniaCurrentMarine Biology 154(4)649ndash659 DOI 101007s00227-008-0958-3

Brown JL 1964 The evolution of diversity in avian territorial systemsWilson Bulletin76160ndash169

Calder DR 1982 Life history of the cannonball jellyfish Stomolophus meleagrisL Agassiz 1860 (Scyphozoa Rhizostomida) Biological Bulletin 162149ndash162DOI 1023071540810

Castro JJ Santiago JA Santana-Ortega AT 2002 A general theory on fish aggregationto floating objects an alternative to the meeting point hypothesis Reviews in FishBiology and Fisheries 11(3)255ndash277 DOI 101023A1020302414472

Ceh J Gonzalez J Pacheco AS Riascos JM 2015 The elusive life cycle of scyphozoanjellyfishmdashmetagenesis revisited Scientific Reports 512037 DOI 101038srep12037

Chirichigno NF Cornejo MU 2001 Cataacutelogo comentado de los peces marinos del PeruacuteCallao Instituto del Mar del Peruacute

Clarke KR Gorley RN 2006 PRIMER v6 user manualtutorial (Plymouth routines inmultivariate ecological research) Plymouth Primer-E Ltd

Clarke KRWarwick RM 1998 Quantifying structural redundancy in ecologicalcommunities Oecologia 113(2)278ndash289 DOI 101007s004420050379

Colin SP Costello JH GrahamWM Higgins III J 2005 Omnivory by the smallcosmopolitan hydromedusa Aglaura hemistoma Limnology and Oceanography50(4)1264ndash1268 DOI 104319lo20055041264

Connell JH 1963 Territorial behavior and dispersion in some marine invertebratesResearches on Population Ecology 5(2)87ndash101 DOI 101007BF02518833

Corrington JD 1927 Commensal association of a spider crab and a medusa BiologicalBulletin 53(5)346ndash350 DOI 1023071537059

Costa MRD Albieri RJ Arauacutejo FG 2005 Size distribution of the jack Chloroscombruschrysurus (Linnaeus)(Actinopterygii Carangidae) in a tropical bay at SoutheasternBrazil Revista Brasileira de Zoologia 22(3)580ndash586DOI 101590S0101-81752005000300009

Doyle TK Hays GC Harrod C Houghton JD 2014 Ecological and societal benefits ofjellyfish Dordrecht Springer 105ndash127

FischerW Krupp F SchneiderW Sommer C Carpenter KE Niem VH (eds) 1995Guiacutea FAO Para La Identificacioacuten de Especies Para Los Fines de La Pesca Vol 2Rome Organizacioacuten de las Naciones Unidas para la Agricultura y la Alimentacioacuten1136ndash1173

Fleming NE Harrod C Newton J Houghton JD 2015 Not all jellyfish are equalisotopic evidence for inter-and intraspecific variation in jellyfish trophic ecologyPeerJ 3e1110 DOI 107717peerj1110

Greer AT Chiaverano LM Luo JY Cowen RK GrahamWM 2017 Ecology andbehaviour of holoplanktonic scyphomedusae and their interactions with larvaland juvenile fishes in the northern Gulf of Mexico ICES Journal of Marine Science75(2)751ndash763 DOI 101093icesjmsfsx168


Griffin BDT MurphyM 2011 Cannonball jellyfish Stomolophus meleagris (On-line)Available at httpwwwdnrscgov cwcspdfCannonballjellyfishpdf (accessed on 28January 2018)

Gunter G 1935 Records of fishes rarely caught in shrimp trawls in Louisiana Copeia1935(1)39ndash40 DOI 1023071436635

Gutsell JS 1928 The Spider Crab Libinia dubia and the Jelly-fish Stomolophusmeleagris found Associated at Beauford North Carolina Ecology 9(3)358ndash359DOI 1023071932377

Haddock SHD 2008 Reconsidering evidence for potential climate-related increases injellyfish Limnology and Oceanography 532759ndash2762 DOI 104319lo20085362759

Hargitt CW 1904 The medusae of the Woods Hole Region Bulletin of the Bureau ofFisheries 2421ndash79

Hildebrand HH 1954 A study of the Fauna of the brown shrimp (Penaeus aztecus Ives)grounds in the western Gulf of Mexico Univ Tex Pub Inst Mar Sci 3(2)233ndash366

Hobbs J-PA Munday PL 2004 Intraspecific competition controls spatial distributionand social organisation of the coral-dwelling goby Gobiodon histrioMarine EcologyProgress Series 278253ndash259 DOI 103354meps278253

Hoese HD Copeland BJ Miller JM 1964 Seasonal occurrence of Cyanea medusae in theGulf of Mexico at Port Aransas Texas Texas Journal of Science 16(3)391ndash393

HornMH 1970 Systematics and biology of the stromateid fishes of the genus PeprilusBulletin of the Museum of Comparative Zoology 140(5)165ndash261

Ingram BA Pitt KA Barnes P 2017 Stable isotopes reveal a potential kleptoparasiticrelationship between an ophiuroid (Ophiocnemis marmorata) and the semaeostomejellyfish Aurelia aurita Journal of Plankton Research 39(1)138ndash146DOI 101093planktfbw088

Institute of Hydrology Meteorology and Environmental Studies (IDEAM) 2004Caracterizacioacuten climaacutetica de variables oceacuteano atmosfeacutericas sobre la cuenca delPaciacutefico colombiano (on-line) Available at httpwwwideamgovcodocuments2102123877 clima+pacificopdf e5e74fd3-67da-406e-968e-4d34d34e3f12 (accessedon 18 December 2017)

Javidpour J Cipriano-Maack AN Mittermayr A Dierking J 2016 Temporal dietaryshift in jellyfish revealed by stable isotope analysisMarine Biology 163(5)Article 12DOI 101007s00227-016-2892-0

Jordan DS Evermann BW 1898 The fishes of North and Middle America WashingtonBull US Nat Mus Smithsonian Institution TFH Publications

Kraeuter JN Seltzler EM 1975 The seasonal cycle of Scyphozoa and Cubozoa inGeorgia estuaries Bulletin of Marine Science 25(1)66ndash74

Larson RJ 1991 Diet prey selection and daily ration of Stomolophus meleagris a filter-feeding scyphomedusa from the NE Gulf of Mexico Estuarine Coastal and ShelfScience 32(5)511ndash525 DOI 1010160272-7714(91)90038-D

Lazarus JF Cantera JR 2007 Crustaacuteceos (Crustacea Sessilia Stomatopoda IsopodaAmphipoda Decapoda) de Bahiacutea Maacutelaga Valle del Cauca (Paciacutefico colombiano)Biota Colombiana 8221ndash190


LoacutepezMJ Rodriacuteguez RJ 2008 First record of association of the blackfin jackHemicaranx zelotes with the cannonball jellyfish Stomolophus meleagris in Kino BayGulf of California Hidrobiologica 18173ndash176

Lynam CP Brierley AS 2007 Enhanced survival of 0-group gadoid fish under jellyfishumbrellasMarine Biology 1501397ndash1401 DOI 101007s00227-006-0429-7

Lynam CP GibbonsMJ Axelsen BE Sparks CA Coetzee J Heywood BG BrierleyAS 2006 Jellyfish overtake fish in a heavily fished ecosystem Current Biology16(13)R492ndashR493 DOI 101016jcub200606018

Martin BD Schwab E 2013 Current usage of symbiosis and associated terminologyInternational Journal of Biology 5(1)32ndash45

Martinelli JE Stampar SN Morandini AC Mossolin EC 2008 Cleaner shrimp(Caridea Palaemonidae) associated with scyphozoan jellyfish Vie et milieu-Life andEnvironment 58(2)133ndash140

Morton B 1989 Partnerships in the sea Hong Kong Hong Kong University Press 140Nagata RMMoreira MZ Pimentel CR Morandini AC 2015 Food web characterization

based on δ15N and δ13C reveals isotopic niche partitioning between fish andjellyfish in a relatively pristine ecosystemMarine Ecology Progress Series 51913ndash27DOI 103354meps11071

Naman SM Greene CM Rice CA Chamberlin J Conway-Cranos L Cordell JR Hall JERhodes LD 2016 Stable isotope-based trophic structure of pelagic fish and jellyfishacross natural and anthropogenic landscape gradients in a fjord estuary Ecology andEvolution 6(22)8159ndash8173 DOI 101002ece32450

Ohtsuka S Koike K Lindsay D Nishikawa J Miyake H KawaharaMMujiono NHiromi J Komatsu H 2009 Symbionts of marine medusae and ctenophoresPlankton and Benthos Research 41ndash13 DOI 103800pbr41

Padilla-Serrato JG Loacutepez-Martiacutenez J Acevedo-Cervantes A Alcaacutentara-Razo ERaacutebago-Quiroz CH 2013 Feeding of the scyphomedusa Stomolophus meleagris inthe coastal lagoon Las Guaacutesimas northwest Mexico Hidrobioloacutegica 23(2)218ndash226

Page JW 2015 Characterization of bycatch in the cannonball jellyfish fishery inthe coastal waters off GeorgiaMarine and Coastal Fisheries 7(1)190ndash199DOI 1010801942512020151032456

Pauly D GrahamW Libralato S Morissette L Palomares MD 2009 Jellyfish inecosystems online databases and ecosystem models Hydrobiologia 616(1)67ndash85DOI 101007s10750-008-9583-x

Phillips PJ BurkeWD Keener EJ 1969 Observations on the trophic significance ofjellyfishes in Mississippi Sound with quantitative data on the associative behav-ior of small fishes with medusae Transactions of the American Fisheries Society98(4)703ndash712 DOI 1015771548-8659(1969)98[703OOTTSO]20CO2

Phillips PJ Levin NL 1973 Cestode larvae from scyphomedusae of the Gulf of MexicoBulletin of Marine Science 23(3)574ndash584

Pitt KA Clement AL Connolly RM Thibault-Botha D 2008 Predation by jellyfishon large and emergent zooplankton implications for benthicndashpelagic couplingEstuarine Coastal and Shelf Science 76(4)827ndash833 DOI 101016jecss200708011


Pitt KA Connolly RMMeziane T 2009 Stable isotope and fatty acid tracers inenergy and nutrient studies of jellyfish a review Hydrobiologia 616(1)119ndash132DOI 101007s10750-008-9581-z

Poveda G Jaramillo L Vallejo LF 2014 Seasonal precipitation patterns along path-ways of South American low-level jets and aerial riversWater Resources Research50(1)98ndash118 DOI 1010022013WR014087

Prahl HV Cantera JR Contreras R 1990 Manglares y hombres del Paciacutefico colom-biano (No 33391809861 P898) Fondo Colombiano de Investigaciones Cientiacuteficasy Proyectos Especiales (Colombia) Ministerio de Educacioacuten Nacional (Colombia)

Purcell JE Arai MN 2001 Interactions of pelagic cnidarians and ctenophores with fish areview Hydrobiologia 45127ndash44 DOI 101023A1011883905394

Riascos JM Cantera JR Blanco-Libreros JF 2018 Growth and mortality of mangroveseedlings in the wettest Neotropical mangrove forests during ENSO implications forvulnerability to climate change Aquatic Botany 14734ndash42DOI 101016jaquabot201803002

Riascos JM CuturrufoM Pacheco AS Oliva ME 2011 Regulatory factors and structureof a component population of the spionid Polydora bioccipitalis infesting the surfclamMesodesma donacium Journal of Aquatic Animal Health 23(3)125ndash133DOI 101080089976592011616845

Riascos JM Heilmayer O Laudien J 2008 Population dynamics of the tropical bivalveCardita affinis from Maacutelaga Bay Colombian Pacific related to La Nintildea 1999ndash2000Helgoland Marine Research 62(1)S63ndashS71 DOI 101007s10152-007-0083-6

Riascos JM Vergara M Fajardo J Villegas V Pacheco AS 2012 The role of hyperiidparasites as a trophic link between jellyfish and fishes Journal of Fish Biology81(5)1686ndash1695 DOI 101111j1095-8649201203427x

Riascos JM Villegas V Caacuteceres I Gonzalez JE Pacheco AS 2013 Patterns of a novelassociation between the scyphomedusa Chrysaora plocamia and the parasiticanemone Peachia chilensis Journal of the Marine Biological Association of the UnitedKingdom 93(4)919ndash923 DOI 101017S002531541200094X

Riascos VJM 2006 Effects of El Nintildeo-Southern oscillation on the population dynamicsof the tropical bivalve Donax dentifer from Maacutelaga Bay Colombian PacificMarineBiology 1481283ndash1293 DOI 101007s00227-005-0165-4

Richardson AJ Bakun A Hays GC GibbonsMJ 2009 The jellyfish joyride causesconsequences and management responses to a more gelatinous future Trends inEcology and Evolution 24312ndash322 DOI 101016jtree200901010

Robertson DR Allen GR 2015 Shore fishes of the Tropical Eastern Pacific onlineinformation system Version 20 Smithsonian Tropical Research Institute BalboaPanamaacute

Rountree RA 1983 The ecology of Stomolophus meleagris the cannon jellyfish and itssymbionts with special emphasis on behaviour Honors thesis The University ofNorth Carolina at Wilmington NC (USA)

Sanz-Martiacuten M Pitt KA Condon RH Lucas CH Novaes de Santana C Duarte CM2016 Flawed citation practices facilitate the unsubstantiated perception of a


global trend toward increased jellyfish blooms Global Ecology and Biogeography25(9)1039ndash1049 DOI 101111geb12474

Shanks AL GrahamWM 1988 Chemical defense in a scyphomedusaMarine EcologyProgress Series 4581ndash86

Smith HM 1907 The fishes of North Carolina volume 2 Raleigh North Carolinageological and economic survey

Sullivan LJ Gifford DJ 2004 Diet of the larval ctenophore Mnemiopsis leidyi AAgassiz (Ctenophora Lobata) Journal of Plankton Research 26(4)417ndash431DOI 101093planktfbh033

Tunberg BG Reed SA 2004Mass occurrence of the jellyfish Stomolophus meleagrisand an associated spider crab Libinia dubia Eastern Florida Florida Scientist67(2)93ndash104

Vannucci M 1954Hydrozoa e Scyphozoa existentes no instituto oceanograacutefico IIBoletim do Instituto Oceanograacutefico 5(1ndash2)95ndash149DOI 101590S0373-55241954000100005

Whitten HL Rosene HF Hedgepeth JW 1950 The invertebrate fauna of Texas coast jet-ties a preliminary survey Publications of the Institute of Marine Science 1(2)53ndash100


resourcersquorsquo that potentially increases the survival and recruitment of the symbionts tothe adult population We argue that if this outcome of the symbiotic association canbe proven scyphozoan jellyfish can be regarded as floating nurseries

Subjects Biodiversity Ecology Marine Biology Population BiologyKeywords Jellyfish blooms Feeding ecology Fisheries Scyphozoans Gelatinous zooplanktonFish recruitment Symbiosis Diversity of interactions Trophic ecology Estuaries

INTRODUCTIONThe magnitude and frequency of population blooms of jellyfish (pelagic cnidarian andctenophores) are seemingly increasing along with strong impacts on marine ecosystemsThe collapse of formerly rich fisheries has been linked to increasing jellyfish populationsin several regions (Lynam et al 2006 Brodeur Ruzicka amp Steele 2011) However much ofthe societal and even scientific perception about jellyfish and their role in ecosystems isbased on speculation limited evidence and flawed scientific practices (eg Haddock 2008Richardson et al 2009 Sanz-Martiacuten et al 2016) Trophic interactions between jellyfish andplanktivorous fishes have been characterized as a combination of mutual predation andcompetition for planktonic food (Purcell amp Arai 2001 Lynam et al 2006 Brodeur et al2008 Richardson et al 2009) Changes in the balance of these trophic pathways in stressedand overfished ecosystems have been hypothesized to explain massive local proliferationsof jellyfish that displace planktivorous fishes and form alternate jellyfish-dominatedecosystems (Richardson et al 2009) However trophic relationships are only known for asmall portion of this polyphyletic assemblage spanning more than 2000 species (Fleming etal 2015) As a result trophic models assessing food web structure and energy flow oftenignore jellyfish or include them as a single functional group with the characteristics of anlsquoaveragersquo jellyfish whose parameterization frequently varies greatly among models (Paulyet al 2009) In fact the hypotheses proposed to explain changes in jellyfish dominatedecosystems remain untested partially because there is a recognition thatmore basic researchon feeding ecology is still required (Pauly et al 2009 Richardson et al 2009 Naman et al2016)

Regarding scyphozoan jellyfish two emerging issues are challenging the predominantview of competitive trophic interactions between planktivorous fishes and jellyfish Firstrecent methodological approaches have shown that scyphozoans use unsuspected foodsources including benthic organisms (Pitt et al 2008 Ceh et al 2015) microplanktonand resuspended organic matter (Javidpour et al 2016) These food sources have beentraditionally overlooked because most studies on feeding ecology use gut content analysisthat focuses on mesozooplankton and ichthyoplankton presumably because they aremore visible and retained in the gut for longer than other type of food (Pitt Connolly ampMeziane 2009) Thus the widely held view that fishes and scyphozoan jellyfish competefor the same food source seems a gross generalization Second mounting evidence suggeststhat mutual predation (ie medusae predating on fish egg or larvae and fishes predatingon medusae early life stages) is only one side of the story Scyphozoans usually display



























Ciliophora 0 (0) 0 (0) 0 (0) 0 (0) 06 (16) 0 (0) 64 (143) 0 (0) 0 (0) 0 (0) 46 15



Nematoda 0 (0) 0 (0) 0 (0) 01 (05) 0 (02) 03 (06) 02 (04) 04 (07) 02 (05) 0 (0) 19 06



Unidentified 55 (21) 115 (64) 45 (46) 43 (4) 22 (34) 32 (48) 48 (38) 3 (29) 25 (31) 06 (09) 386 125


Riascos


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0

20

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60

80

100

120

140

0

5

10

15

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25

30

D J 2016 F M A M

Mean b

ell

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r (m

m)

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D

Rela

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bundance (

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-1)

A

0

20

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60

80

100

120

0

5

10

15

20

25

30

D J 2017 F M A M

Mean b

ell

dia

mete

r (m

m)

+S

D

Rela

tive a

bundance (

ind h

-1)

B







2D Stress 026

Dec

Jan

Feb

Mar

Apr

May

Season 1

Jan

Feb

Mar

Apr

Season 2
















-010 -005 0 005 010 015

CAP1

-010

-005

0

005

010

015

C A

P 2

Feb

Mar

Apr

Season 2

Feb

Mar

Apr

May

Season 1








0

20

40

60

80

100

120

140

160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)


Hemicaranx zelotes



























Table 4 (continued)















































































































































Ciliophora 0 (0) 0 (0) 0 (0) 0 (0) 06 (16) 0 (0) 64 (143) 0 (0) 0 (0) 0 (0) 46 15



Nematoda 0 (0) 0 (0) 0 (0) 01 (05) 0 (02) 03 (06) 02 (04) 04 (07) 02 (05) 0 (0) 19 06



Unidentified 55 (21) 115 (64) 45 (46) 43 (4) 22 (34) 32 (48) 48 (38) 3 (29) 25 (31) 06 (09) 386 125


Riascos


622

0

20

40

60

80

100

120

140

0

5

10

15

20

25

30

D J 2016 F M A M

Mean b

ell

dia

mete

r (m

m)

+S

D

Rela

tive a

bundance (

ind h

-1)

A

0

20

40

60

80

100

120

0

5

10

15

20

25

30

D J 2017 F M A M

Mean b

ell

dia

mete

r (m

m)

+S

D

Rela

tive a

bundance (

ind h

-1)

B







2D Stress 026

Dec

Jan

Feb

Mar

Apr

May

Season 1

Jan

Feb

Mar

Apr

Season 2
















-010 -005 0 005 010 015

CAP1

-010

-005

0

005

010

015

C A

P 2

Feb

Mar

Apr

Season 2

Feb

Mar

Apr

May

Season 1








0

20

40

60

80

100

120

140

160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)


Hemicaranx zelotes



























Table 4 (continued)






















































































































0

20

40

60

80

100

120

140

0

5

10

15

20

25

30

D J 2016 F M A M

Mean b

ell

dia

mete

r (m

m)

+S

D

Rela

tive a

bundance (

ind h

-1)

A

0

20

40

60

80

100

120

0

5

10

15

20

25

30

D J 2017 F M A M

Mean b

ell

dia

mete

r (m

m)

+S

D

Rela

tive a

bundance (

ind h

-1)

B







2D Stress 026

Dec

Jan

Feb

Mar

Apr

May

Season 1

Jan

Feb

Mar

Apr

Season 2
















-010 -005 0 005 010 015

CAP1

-010

-005

0

005

010

015

C A

P 2

Feb

Mar

Apr

Season 2

Feb

Mar

Apr

May

Season 1








0

20

40

60

80

100

120

140

160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)


Hemicaranx zelotes



























Table 4 (continued)






















































































































2D Stress 026

Dec

Jan

Feb

Mar

Apr

May

Season 1

Jan

Feb

Mar

Apr

Season 2
















-010 -005 0 005 010 015

CAP1

-010

-005

0

005

010

015

C A

P 2

Feb

Mar

Apr

Season 2

Feb

Mar

Apr

May

Season 1








0

20

40

60

80

100

120

140

160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)


Hemicaranx zelotes



























Table 4 (continued)
































































































































-010 -005 0 005 010 015

CAP1

-010

-005

0

005

010

015

C A

P 2

Feb

Mar

Apr

Season 2

Feb

Mar

Apr

May

Season 1








0

20

40

60

80

100

120

140

160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)


Hemicaranx zelotes



























Table 4 (continued)






















































































































0

20

40

60

80

100

120

140

160

0 20 40 60 80 100 120

Fish

All

H zelotes

Sym

bio

nt body s

ize (

mm

)


Hemicaranx zelotes



























Table 4 (continued)






































































































































Table 4 (continued)






















































































































floating nurseries? scyphozoan jellyfish, their food and their rich … · 2018-06-19 ·...

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