Historical treatment of jellies: “those @#$%^&* jellies clogged my nets!”

1. SMS 501 Biological Oceanography4 November 2009Mary Jane PerryLecture 17Zooplankton III: Gelatinous Zooplankton AKA Gelly or Jelly Plankton, or Gelata

2. House keepingHighpoints from Marine Waters Conference?Oral final exam schedule – week of finals(in Orono or at the DMC)

3. 1st Law of Thermodynamics – you can’t get something for nothing (photosynthesis uses extraterrestrial energy – from outside earth/ocean system).2nd Law of Thermodynamics – you can’t break evenWhile zooplankton are secondary ‘producers’, there is a cost; efficiency of transfer of consumed POC (phytoplankton or protozoa or other organic particle) to new zooplankton body mass or eggs is ~ 10- 15%.

4. Copepods dominate zooplankton biomass in many places.Zooplankton have ‘behaviors’ – response to chemical or mechanical cues (food or mate or predator); functional response curves for food ingestion as a function of food concentration; heterotrophs are ‘richer’ food.Life scales of months to year +.Time to sexual maturity weeks to months. Growth rate related to temperature and food concentrations.Different strategies of egg production but all related to quantity and quality of food (diatoms & aldehyde production). Swimming speed is scaled to body size; diel migrate vertically.Zooplankton are patchy – aggregation in response to food patches at fronts or thin layers or as predation minimization strategy.Zooplankton control phytoplankton blooms dP = P (growth – loss) dt

5. Zooplankton are typically categorized as crustaceans or gelatinous. Historical treatment of jellies:“those @#$%^&* jellies clogged my nets!”

6. Commerical treatment of jellies2008 Nobel Prize for Green Fluorescent Protein from Aequorea

7. Organisms from 8 phyla are included among the gelata:a) Nemertean. b) Phaeodarian radiolarian.c) Salp w/ parasitic copepod. d) Lobate ctenophore. e) Narcomedusan hydrozoan.f) Nudibranch mollusc. g) Chaetognath. h) Physonect siphonophore. i) Coronate scyphozoan. j) Polychaete. From Haddock. 2004. Hydrobiologia 530/531: 549

8. Gelantinous planktonAKA jelly or gelly plankton; gelatataxonomically very diverse; unified by gelatinous, watery body;transparent (Biol. Bull. 201:113) and fragile; complex life cycles (sexual and asexual reproduction);rapid growth “blooms” with large interannual variability;abundance may be increasing ?diverse feeding patterns:small-particle filter feeders; raptorial predators; sweeping encounter predators

9. Complete transparency only in euphotic zone (not deep sea); note that many gelata are completely transparent. Johnsen, 2001. Biol. Bull. 201: 301

10. Difficult to sample with nets or acoustics.One labor-intensive way is through in situ studies of jellies by divers or observers in submarines

11. Salp volume Salp volume, scaled to crustacean C/vol Gelatinous bodiesmostly transparent (although many deep sea species are bioluminescent); high water content; low nutritional value (low nutritional value and refuge from predation?) *many successful at low food concentrations able to “sweep” or “clear” large volumes of water with low food concentrations at low energy costs (have been called “fake” giants -large filter surface relative to C) can also ‘degrow’ or shrink at very low food conc. (survival)* efficient feeders – compete with zooplankton* high growth rates –> may be responsible for ‘swarms’* tunicates (salps, doliolids, larvaceans) waste products have high sinking rates (material flux) * medusa-like predators not visual predators (compete with fish larvae? do well in regions of turbidity)

12. 3 primary pathways for material & energy flow: * food web(s) leading to large metazoans (i.e., fish) * microbial loop * gelatinous zooplankton – 2 pathways: 1) alternative to microbial loop (small phytoplankton)2) feed on macrozooplankton, but not necessarily a food web leading to fish (can be either raptorial predators or sweeping encounter predators)

13. UrochordatesFilter feeders onsmall particles; tremendous ability to “clear” the water (short circuit microbial loop). Clearance rates comparable to phytoplankton growth rates.Pelagic tunicates Appendicularians or larvaceans – collect particles externally, in a ‘house’Thaliace – filter internallySalps Doliolids They “bloom” but onset of blooms poorly understood

14. Appendicularians (larvacean):Body form of a “tadpole” with tail containing a notochord; hermaphrodites. Forms mucous house which usually surrounds the animal and collects microscopic planktonic particles for consumption. The larvacean can be seen inside or beside the much larger mucous house as it beats its tail to create feeding currents. Vacant houses ––> carbon flux Oikopleura

15. ‘House is a complex set of channels and filters made of mucous fibers and sheets; seawater is pumped by tail to inflate house. Water is pumped into the house by the oscillation of the larvacean's tail. Particles are sieved from the flow as they pass through the internal filter – fine mucus; they accumulate and are aspirated at intervals into the pharynx of the larvacean via a mucous tube. Houses become clogged with particulates and fecal pellets, and are then jettisoned (maybe several times per day). The larvacean expands a new house (there may be several house rudiments on its body, awaiting expansion) and resumes filter feeding. The abandoned houses can be an important source of marine snow and serve as food for various planktonic omnivores. Also can fall to sea floor.’ Madin and Harbison (2001) Encyclopedia of Ocean Sciences, pp. 1120-1130

16. New houses produced w/in a few to 24 hr Sizes from mm to 3 m Abandoned houses sink 800 m/d Larvacean video http://video.google.com/videosearch?q=larvacean&emb=0&aq=f#\

17. Giant larvacean houses: more abandoned houses, more carbon flux. Monterey bay ~ 4 houses/m2 seafloor/day

18. ciliates bacteria flagellates picophytoplankton copepods fish large phytoplankton (diatoms) sinking particles microbial loop and linear food web to fish

19. ciliates bacteria flagellates picophytoplankton copepods fish large phytoplankton (diatoms) larvaceans, salps, doliolids sinking particles larvaceans, etc. short circuit microbial loop  particle export

20. Doliolids:Barrel shaped. Relatively small, transparent body with complete bands of circumferential muscles (8 or 9).Anterior and posterior openings. Feeds on small plankton using currents created by cilia rather than pulsing of body.Hangs motionless until disturbed, and then exhibits characteristic jumpy motion Complex alternation of five asexual and one sexual generations; can occur together as parts of large colonies of thousands of zooids. Colonies may >1m. Fragile, so not collected by nets. Undersampled by acoustics. Madin and Harbison (2001) Encycl. Ocean Sc., pf. 1120

21. Salps:Body with incomplete circular bands of muscles (various numbers depending on the species). Anterior and a posterior opening. Size is mm to cm. Muscular pulsing of body wall pumps water through an internal mucous net that gathers small plankton.Locomotion by jet propulsion, contraction of body muscles. Alternate between two forms – asexually budding solitary (oozooid) stage and a sexually reproducing aggregate (blastozooid) stage. The latter remain connected together in chains or whorls (right figure, chain is 10 m).Growth rates of 0.25 /d. Consume 0.5 body weight / day. Asexuality and rapid growth – important for blooming! Ephemeral, patchy blooms ---- very tough to study ! Madin and Harbison (2001) Encycl. Ocean Sc., pf. 1120

22. A mature solitary stage (oozooid) of salp, Cyclosalpa affinis. Body is oriented so that the oral siphon (i.e. the mouth) is to left. Stolon projects forward from a point just in front of the digestive organs.Files of blastozooids are budded (asexually) and develop along either side of the stolon, the distal ones being more advanced. Lacalli. 1999. Biol. Rev. 74: 177

23. Groups (aggregates) of mature blastozooids then separate to begin an independent life in the plankton. They reproduce sexually (younger chains are female; older colonies are male) to complete the cycle. Each blastozooid in the chain acts as a `nurse' zooid, supporting the growth of a single embryo inside its atrium (left figure). The embryo, when mature, is releases as a solitary stage (oozooid). Growth rates ~ day (similar to phytoplankton). (photo: Gulf of the Farallones NMS) http://www.sanctuaries.nos.noaa.gov/pgallery/pgcordell/living/living_26.html http://www.gcrio.org/ASPEN/epnews/gifs/Salps.gif

24. Thought to be associated with warm water intrusions from Slope Water south of Georges Bank. Absent in 1996, 1997, 1998 (no intrusions? paper does not say).

25. Other regions with documented swarms of salps; up to 100,000 km2(hot spots?)Don’t find swarms in – very low productivity regions (not enough prey for blooms) or – very high productivity regions (clog mucus nets; stop feeding;Harbison et al. 1986)Estimate bloom concentrations to be ~ 1,000 mL biovolume m-2 Madin et al. 2006, DSR I 53: 804

26. Salps graze on wide range of particles, < 2 µm – 1 mmincluding microzooplankton that are not fast enough to escape!Can alter community structure (remove both phyto and zooplankton). Biovolume of Salpa asera of 1,000 mL/m^2 would remove 25% of small particles per night. If phytoplankton double once per day, estimate that salps could remove ~35% of primary production.Sinking rate of fecal pelletsup to 2,700 m d-1(freight-train to the sea floor)! Size matters 

27. Summary pointsParticle size of prey:Urochordates can harvest small cells (alternative to micro loop)Salps (and doliolids) can capture broad range of particles, including microbial loop-sized phytoplankton and small zooplanktonEphemeral blooms Fast reproductive rates – sexual and asexual Rapid growth rates (low resources/ biovolume)Impact on carbon cycle – very fast sinking rate for larvacean houses and salp/doliolid fecal pellets

28. Gelatinous Molluscs: heteropods and pteropod (thecosome and gymnosomes)Reduced shell (no shell in gymnosome pteropods )made of aragonite (CaCO3) – thermodynamically unstable and dissolves more readily than calcite (different crystaline structure)Pteropods are major contributors to global CaCO3 flux.Difficult to sample; net avoidage – heavy and ‘drop’‘Poster’ organism of ocean acidification(ocean is undersaturated with regard to aragonite; decreased pH will drive reaction against formation of aragonite)Depending on species, 2 - 40 mm in length.Generally, poor literature on this group.

29. Heteropod mollusc:Elongate body with single ventrally placed swimming fin, held upward.Light transparent shell (aragonite); some none; fossil record. Sculling motion of fin propels animal forward. Well developed pair of eyes on a snout-like head. Active predators on salps, doliolids, chaetognaths and other gelatinous zooplankton. Different species found at all depths. Difficult to sample. heteropod Oxygyrus

30. Cacavolinia thecosome pteropod (with shell) Thecosome pteropods:Body with large pair of lateral plate-like extensions of foot. Plate flap like wings for propulsion.Some with aragonite calcareous shell, others w/ soft pseudoconch; fossil record.Flux of pteropod shells in Sargasso responds to the annual cycle of primary production in the upper ocean. Jasper and Deuser (1993) DSR I, 40: 653. pH & aragonite

31. Feeding pteropods; Lalli and Gilmer, redrawn in Denny’s (2008) Limacina (shelled pteropod) Herbivores with mucous web to passively collect plankton; it ingests the web (5 sec) and deploys a new one (20 sec). Can also ‘trap’ motile organism in the web, including small copepods. Feeding only observed in situ, by scuba. Web floats above animal, and contributes to buoyancy. Web is ~ 4 times diameter of the organism.

32. Clione gymnosome pteropod Gymnosome pteropods: Body with small pair of lateral muscular wings. Beats wings to swim rapidly.Body lacks any kind of shell. Head with two pairs of retractable antennae and buccal (oral) apparatus with a radula, specialized hook sacs and a jaw. Active predators on thecosome pteropods; juvenile veliger stages feed on phytoplantkon.Sometimes observed in swarms.Few references - Hunt et al. (2008) Prog. Oceanog. 78: 193

33. In the Southern Ocean, Clione limacina antarctica life cycle is strongly synchronized with it’s favorite prey, Limacina helicina antarctica Clione captures Limacina w/ six buccal cones.Proboscis draws body out of shell. Based on Lalli and Gilmer (1989). Original source unknown; http://www.sfu.ca/~fankbone/v/clione01.jpg

35. In Southern Ocean, pteropods are variable but significant part of zooplankton population (I believe data are based on # of individuals; diamonds are maxima observed).Both seasonal and interannual variability in abundances Hunt et al. (2008) Prog. Oceanog. 78: 193

36. Chaetognath (Arrow worms - important predator)Separate phylum2nd in numerical dominance to copepodsSlender transparent body, large caudal fin, anterior spines of either side of mouth. Carnivorous - catch large numbers of zooplankton and swallow them whole; ambush or raptorial feeders; sense hydrodynamic signals from prey.Mechanoreceptors to sense water movement and detect prey; behavior of prey will influence selectivity (active vs. passive prey).Can eat large copepods (major predator); capture efficiency related to prey escape; primarily feed on copepodites.Can be cannibals, particularly late in season (leads to rapid population decline).

37. Chaetognath head with spines -->>

38. Table shows % prey population removed per day – seasonally, big impact on prey populations Functional response curve: more prey -> more consumption; not satiated in this experiment. Voracious carnivores http://video.google.com/videosearch?hl=en&resnum=0&q=chaetognath&um=1&ie=UTF-8&sa=N&tab=wv# Tonnesson and Tiselius 2005MEPS 289: 177

39. What is the role of predators like chaetognaths in regulating zooplankton populations (top-down control?) Central-West North Sea (5 mi from English coast) omnivore abundance predator abundance Note seasonal switch of dominant predator from ‘jelly fish’ (Hydroida / medusa) to Chaetognatha (gelata are major predator)s. Clark et al. 2003. ICES J. Mar. Science 60: 187

40. What is the role of predators like chaetognaths in regulating zooplankton populations (top-down control?) Central-West North Sea (5 mi from English coast) omnivore abundance predator abundance Is summer decrease in omniovores (mostly copepods) due to Chaetognatha? Clark et al. 2003. ICES J. Mar. Science 60: 187

41. Ctenophores (sea gooseberries):Body with 8 rows of combs (ciliary plates), often seen as shimmering waves of color. Usually transparent (except for some of the deep-water forms). Predators on various types of zooplankton, fish eggs, planktonic larvae.Suspension feeders (of sorts), sweeping two contractile tentacles. No stinging cells; colloblasts on tentacles secrete a sticky substance to entangle prey. When contact a prey, tentacles contract and pass food to mouth. Bioluminescent – typically green light.

42. Ctenophore body shapes. Some exceed a meter and can only be collected by divers or submarines.Haddock. 2004. Hydrobiologia 530:549: 549

43. Bolinopsis ctenophore

44. Laurence P. MadinBolinopsis vitrea, a lobate ctenophore

45. Pleurobrachiactenophore

46. Unidentified CtenophorePhoto by MarshYoungbluth

47. Gellies are difficult to quantitatively sample;example of using fish as integrator – stomach content and frequency of occurrence of ctenophores; NW Atlantic (region, next slide) Link and Ford, 2006, MEPS 320: 153

48. 1981 1986 1991 1996 Climate change?Climate oscillations? Is this a permanent change in distributional pattern?Or in prey preference?

49. Beroe ovataLater introduced into the Black Sea, in ballast water; predator on Mnemiopsis. Here with mouth open.http://www.imagequest3d.com/pages/general/news/blackseajellies/blackseajellies.htm Mnemiopsis leidyi Introduced into the Black Sea in 1982, presumably in ballast water; predator on zooplankton

50. Historical background of Blank Sea: By 1970, overfishing removed top pelagic predators. Went from 4 trophic levels to 3. Daskalov et al. (2007) PNAS 104: 10,518 Small planktivorous fish increased (large fish predation pressure was removed); fishery developed for small fish. By 1980’s, small fish were overfished. Zooplankton increased (small fish predation pressure was removed). In 1982, Mnemiopsis was introduced by ballast water into Black Sea. Abundant food (zooplankton) and no predator (small fish gone) ––> population explosion (at one time Mnemiopsis was 90% of animal biomass in Black Sea ! ). Phytoplankton increased (zooplankon predation pressure gone). Algal blooms w/o grazing ––> anoxia. Fertilizer runoff ‘helped’. W/o fishing, small fish ‘recovered’, exerting predation on zooplankton. Beroe, predator on Mnemiopsis introduced in ballast.