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Tuesday, 14 June 2016

Jellyfish


The word “jellyfish” is a popular term defining what marine biologists call gelatinous macrozooplankton. The word “gelatinous” refers to the general consistency of these animals: their body is mostly made of extracellular matrix (often called mesoglea), i.e. the matrix that holds cells together and that is present in all animals, including us, but that, in these organisms, is the greatest portion of the whole body. Jelly refers just to gelatine. This body architecture is shared by animals that are very far from each other, in terms of evolutionary history. The fossil record tells us that true jellyfish are the oldest animals among those that are still living today, being represented in fossils that date back to the Pre-Cambrian. They are referred to the phylum Cnidaria (Cartwright et al., 2007). Vertebrates, including us, are referred to the phylum Chordata, and some chordates, namely the Tunicata, are also members of gelatinous macrozooplankton, with the Thaliacea and the Appendicularia. Gelatinous macrozooplankton, furthermore, comprises also the Ctenophora, or comb jellyfish. The representatives of these three phyla are the bulk of gelatinous macrozooplankton and, together, make up what we call “jellyfish” (Boero et al., 2008). The following paragraphs contain a textbook-knowledge account of the three phyla, summarizing the information that is relevant for the scopes of this report.

Cnidaria 

The true jellyfish are the planktonic stages of three cnidarian classes: the Hydrozoa, the Scyphozoa, and the Cubozoa. Most Scyphozoa and all Cubozoa fall within the category of macro- and even megazooplankton, since they are large enough, as adults, to be perceived by the naked eye, ranging from 2 mm (e.g. some small medusae) to 2 m in bell diameter, and several metres of tentacle length, of the largest medusae. Some Hydrozoa are macroplankters too, but many species belong to the mesozooplankton, being smaller than 2 mm. Gelatinous mesozooplankton is usually not perceived by a casual observer, unless when its representatives reach high densities. Jellyfish move by jet propulsion, contracting their bells, or umbrellas. The umbrella usually carries tentacles on its margin and has a manubrium hanging in its cavity. The mouth is at the end of the manubrium. The tentacles catch the prey and bring it to the manubrium. Cnidarians do have stinging cells, i.e. cells armed with cnidocysts, little capsules containing an inverted filament that can be everted to inject a venom into their victims (either preys or predators or... us). With very few exceptions, cnidarian jellyfish are carnivores, and use their cnidocysts to kill their prey that, according to the species, can be either other jellyfish, or crustaceans, or fish eggs and larvae, or anything reaching a viable size for the predator. Some, however, are microphagous or even contain zooxanthellae. Cnidarian jellyfish, also called medusae, have complex life cycles that often involve a benthic stage: the polyp. Jellyfish life histories often involve larval amplification. The adult medusae reproduce sexually, and each fertilization leads to the formation of a planula larva (Fig. 1).


The larva settles and leads to a colony that can become quite large, feeding on other animals. A single colony, through asexual reproduction, can produce thousands of small medusae that, then, will grow to maturity. “Amplification” means that each fertilization event does not lead to a single adult but, instead, to many adults, due to asexual reproduction in the polyp stage. The sexually competent medusa is the adult, whereas the polyp stage, where the amplification occurs, is a larva. Hence: larval amplification. Many Hydrozoan species have suppressed the medusa stage and are sexually mature as polyps. Whereas some Hydrozoans and Scyphozoans do not have a polyp stage, and spend their whole life as medusae. The Hydrozoa produce medusae by lateral budding, the Scyphozoa by strobilation, and the Cubozoa by complete metamorphosis of a polyp into a medusa. Besides medusae, the Cnidaria can contribute to gelatinous macrozooplankton as floating or swimming colonies, such as the hydroids Velella and Porpita, or siphonophores like Physalia. 
1.1.2. Ctenophora Gelatinous macrozooplankton is usually equated to stinging jellyfish, and its presence causes major concern about own safety in non-marine biologists, due to fear of potential stings. Many members of gelatinous zooplankton, however, are not Cnidaria, and do not sting. The Ctenophores (Fig. 2) do not have a bell and a manubrium, and do not move by pulsations, they just share a gelatinous appearance with the Cnidaria. Ctenophores move by ciliary propulsion, through what zoologists call “ctenes” or combs. Hence the popular name: comb jellies. They 3 can be a few centimetres, or even 50 or more centimetres, being globular, or similar to a dirigible, or ribbon like. Ribbon like ones, of the genus Cestum, can move also by snake like movements, but the other members of the group usually glide, appearing motionless and, in spite of that, moving. Their bodies are characterized by iridescent glows that are caused just by the flapping combs, the propulsors of the animal. Ctenophores have two tentacles armed with colloblasts, cell organelles that, instead of containing a venom, as the cnidocytes of Cnidaria, contain a glue that holds on their victims. Like cnidarian jellyfish, they also feed on other gelatinous plankters, on crustaceans, or on fish eggs and larvae, being comparable to true jellyfish in their feeding habits. Ctenophores have no impact on human health, and cannot cause any direct harm to us. Ctenophores are holoplanktonic (some are benthic, but will not be considered in the present account), there whole life cycle taking place in the water column. 1.1.3. Chordata Pelagic tunicates (Fig. 3) are members of the phylum Chordata; they comprise the Thaliacea and the Larvacea, or appendicularians. The Larvacea are of small size, but can be present in very high quantities. The Thaliacea, namely salps, doliolids and pyrosomes, are of much larger size, pyrosome colonies and salp chains reaching several metres in length. Pelagic tunicates are much different from both Cnidaria and Ctenophora in their feeding habits, they are filter feeders upon protists (usually phytoplankton), bacteria and even viruses. Their life cycles are holoplanktonic and involve both sexual and asexual reproduction, with the possibility of high biomass increases due to formation of large colonies. Apparently, just as for Ctenophora, the pelagic tunicates do not have benthic stages. Figure 2. A ctenophore: Leucothoea (art by A. Gennari). Figure 3. A pelagic tunicate: Salpa (art by A. Gennari). 4 1.2. The blooms The whole functioning of marine ecosystems is based on blooms, i.e. on pulses of primary and secondary production due to the sudden increase in the population size of some key species. The spring bloom of phytoplankton, in temperate seas like the Mediterranean and the Black Seas, is determined by a peak of primary production of planktonic protists (the phytoplankton) that are usually diatoms or flagellates. The phytoplankton pulse is followed by a zooplankton pulse that takes advantage of the phytoplankton. Crustaceans, especially copepods, are the main representatives of herbivorous zooplankton. The zooplankton peak sustains the rest of the food web, being predated upon by carnivorous plankters. Among these, fish larvae and juveniles are prominent, eventually to become the well-known representatives of nekton: the fish. The pathway phytoplankton → herbivorous crustacean zooplankton → carnivorous zooplankton → fish (Fig. 4) is the backbone of marine production and sustains also our exploitation of marine resources, through fisheries. The species forming the nodes of this pathway are part of a system that functions due to production pulses (the blooms). If the pathway is sustained, the ecosystem produces fish that, in their turn, realize complex pathways within the fish universe. Small fish are fed upon by larger fish, and most of the nekton seems to be self-sufficient. But this is just an impression. Primary production must be at the base of food webs, and primary production is mainly the phytoplankton pulses. The impression of self-sufficiency of the fish domain reveals its weakness if we consider fish as life cycles, and not just as the adults we feed upon. Fish larvae and juveniles are often carnivorous, but they feed on preys that are herbivorous: the copepods and other crustaceans that rely on the phytoplankton pulses. An ecosystem cannot function with carnivores only! Figure 4. The pathway phytoplankton → herbivorous crustacean plankton → carnivorouszooplankton → fish (art by A. Gennari, graphics by F. Tresca). 5 1.3. Ecosystem “malfunctioning” The term “malfunctioning” is obviously anthropocentric. All ecosystems do function, otherwise they would cease to exist. If they function so as to satisfy our expectations, they are considered as functioning well, whereas if they cease to do so, then they are labeled as functioning in a bad way (malfunction means just this: bad functioning). Jellyfish are the oldest animals, among the ones that are currently present on the planet. They were present since the Pre-Cambrian and are not so different from their ancestors. Having passed through more than 500 millions of years of natural selection, with no big changes in their body organization, these animals are simply perfect! Simple and perfect. They also express their populations in pulses, like most of the representatives of marine systems. Jellyfish blooms, thus, are a quite normal phenomenon. The evolution of highly efficient animals, such as fish, however, probably posed a limit to their prevalence in the oceanic realm, with the triumph of the phytoplankton → herbivorous crustacean zooplankton → fish pathway that we like so much. A system based on pulses, however, is almost reset at each seasonal cycle. Such systems have been called “lottery systems” (see Boero, 1994; Fraschetti et al., 2003 for reviews). There is a “prize”, represented by the primary production pulse, and the winners are those who better utilize it, channeling its energy into their representatives, so as to build another pulse. For the fish to be the winners, their larvae and juveniles must tap from the secondary production of crustaceans. Jellyfish compete with the fish larvae and juveniles for the use of this resource. Furthermore, they can also feed on the eggs and larvae of the fish. We have seen that jellyfish have life cycles with larval amplification (Fig. 1). They can be produced in great quantities, so as to rapidly build huge populations. Hence: jellyfish blooms. The lottery game in marine systems is based on the match or mismatch of the secondary or tertiary producers with the pulses that are at the base of marine ecosystems (Cushing, 1990). If the jellyfish produce a pulse with a good match with the pulse of crustaceans, and the fish do not, then the jellyfish can take over, and their bloom is reinforced. The bloom of jellyfish will compete with the fish larvae and juveniles and limit their growth, but it can also impact directly on the fish, since the blooming jellyfish will predate also on their eggs and larvae (Moller, 1984). When this happens, the phytoplankton → herbivorous crustacean zooplankton → fish pathway is disrupted, with the onset of the phytoplankton → herbivorous crustacean zooplankton → jellyfish pathway (Fig. 5). Figure 5. The pathway phytoplankton → crustacean plankton → jellyfish (art by A. Gennari, graphics by F. Tresca). 6 The fish, however, can rely on their “internal” pathways and most of them can stand the failure of one cohort, since they are long lived and can spawn for several years. The loss of one cohort can be buffered by the adult individuals that, usually, are invulnerable to jellyfish or that even feed upon them. Jellyfish, instead, are short lived and the individuals that make up a single pulse cannot persist and must reproduce successfully, starting from scratch, to produce another pulse in the subsequent favorable season. Fish, instead, can “hold their breath” and try again a year later. When systems work in this way, jellyfish blooms are “accidents” that do not disrupt in a radical way the functioning of the phytoplankton → herbivorous crustacean zooplankton → fish pathway. Hence they can be disregarded, as they have been so far by fisheries biologists. They have an impact, of course, but of limited entity. The “jellyfish” considered here are the carnivorous ones, namely Cnidaria and Ctenophora. The same pattern can be present also for herbivorous jellyfish, namely the Chordata. They feed directly on the phytoplankton and when they are particularly abundant they compete with the copepods, depleting the phytoplankton → herbivorous crustacean zooplankton → fish pathway, with the production of a short circuit in it: the phytoplankton → herbivorous gelatinous zooplankton pathway (Fig. 6). At the end of their peak, pelagic tunicates usually contribute to what we call marine snow and fall to the benthos, almost skipping the pelagic trophic pathways (besides the bacteria that feed on them while they are falling towards the bottom). Figure 6. The pathway phytoplankton → herbivorous gelatinous zooplankton (art by A. Gennari, graphics by F. Tresca). 7 1.4. The grand picture Marine ecosystems functioning, thus, takes place through three main pelagic pathways: the phytoplankton → herbivorous crustacean zooplankton → carnivorous zooplankton → fish pathway, the phytoplankton → herbivorous crustacean zooplankton → carnivorous gelatinous zooplankton pathway, and the phytoplankton → herbivorous gelatinous zooplankton pathway (Fig. 7). These pathways are not mutually exclusive, but one can prevail over the others. Usually, the first one (ending up with fish) prevails and determines what we consider as a “normal” situation (Fig. 4). The other two pathways, one ending up with carnivorous gelatinous zooplankton (Fig. 5) and the other with herbivorous gelatinous zooplankton (Fig. 6), from time to time can go through episodic success that, normally, cannot disrupt the prevailing pathway, ending up with fish. These blooms might even enhance the diversity in the nekton, as hypothesized above. The scientific literature is replenished of records of “anomalous” blooms of gelatinous plankton that, traditionally, have been considered as freaks in the functioning of marine systems. As a matter of fact, they are not freaks, they are part of the manifold possibilities in which marine ecosystems work. The evolutionary lineages interacting in these systems coexist since millions of years and can cope with each other. Figure 7. The three main pathways determining marine ecosystem functioning (art by A. Gennari, graphics by F. Tresca). 8 1.5. The impact of gelatinous plankton on fish populations Summarizing, the impact of gelatinous zooplankton on fish populations can be: i) positive, due to a keystone effect that prevents the monopolization of overly successful fish species at the expenses of others, so maintaining fish biodiversity high. This effect occurs when fish and jellyfish coevolved in the same environmental context and if the jellyfish are abundant just for short periods; ii) negative, due to predation on and competition with fish larvae and juveniles (predation occurs also on fish eggs) if the jellyfish are not coevolved with the resident fish or if the fish populations are not “healthy”, due to overfishing, and the jellyfish blooms are abnormally large and long-lasting. A different kind of competition might be exerted by thaliaceans, since they overexploit the phytoplankton and deplete resources for the crustacean grazers that are fed upon by fish larvae and juveniles. 1.6. Measures and estimates of predation impacts of gelatinous plankton on fish The species of gelatinous plankton are in the thousands, and most of them are Hydromedusae (see Bouillon et al., 2004; Bouillon et al., 2006), followed by the Scypozoa and Cubozoa (see Arai, 1997), the Tunicata (see Bone, 1998), and the Ctenophora (see Harbison et al., 1978). In comparison to the very high diversity of this compartment of plankton, the number of species whose biology and ecology have been investigated is exceedingly small. For most of them we barely know that they exist, and often even their life cycles are unknown. These predators, furthermore, are very opportunistic since they are equipped with tentacles armed with cnidocysts or colloblasts that can catch almost anything, from unicellular organisms to much larger prey. Some are very specialized in their diets, but most of them feed on anything they can find. The study of the trophic role of gelatinous plankton, and especially the carnivorous one, is made in two ways. The simplest one consists in collecting animals in the field and inspecting their gut, listing all the food items they contain. Feeding rates are measured in the laboratory, offering food to the animals and evaluating their clearing rates from a given volume of water and the time of digestion of the offered prey. These studies have been made on few species and at specific places (Tab I and II for Aurelia aurita). If a jellyfish species lives both in the North Sea and in the Mediterranean Sea, as is the case of Pelagia noctiluca (Tab. III), the study of its diet in the North Sea does not necessarily reflect its diet in the Mediterranean Sea, since the available food items might be very different. So, what has been found at one place cannot be automatically extended to all the places where a given species occurs. 

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