Physalia utriculus are known in Australia as “blue bottles”. Blue bottles have a characteristic transparent float and tentacles that have a bright blue or purplish coloration. Mature individuals usually grow up to 15 cm in length. They are often mistaken by the larger Atlantic species Physalia physalis (Portuguese man o’ war), whose individuals can reach up to 13 metres in length.

They are commonly found along the shoreline on the beaches of Queensland between the months of November and March, especially during strong northeasterly wind conditions. In January 2019, Surf Life Saving QLD reported more than 13000 stings over a single week (Palin, 2019). Groups of blue bottles are called “armadas” (Spanish and Portuguese; naval fleet). Large armadas of blue bottles and Velella velella (“by-the-wind sailor”) on Queensland’s waters can cause several beaches to close during the Australian summer.

P. utriculus belongs to the phylum Cnidaria, class Hydrozoa and order Siphonophora. Most hydrozoans undergo alternation of generations, and P. utriculus is not an exception, with asexual sessile polyps that develop into sexual planktonic medusae. P. utriculus is a colonial siphonophore composed of both polypoid and medusoid individuals with specialised zooids. Gastrozooids aid in feeding and digestion, dactylozooids form the tentacles and are used for prey capture and defence and gonozooids perform reproductive functions. (Brusca, Moore and Shuster, 2016)

Physalia utriculus (blue bottle). Gold Coast 2019

Blue bottles have a pneumatophore (or float); a double-walled gas chamber lined with chitin that can grow up to 15 cm in length. Each float houses a gland which secretes a gas usually similar to air in composition, although in Physalia it includes a surprisingly high proportion of carbon monoxide. The amount varied from 0.21% to 6.07% of the total in Physalia physalis. It is suggested that variations in carbon monoxide content may reflect differing functional states in the organism. The composition of the gas in the pneumocyst may change qualitatively and quantitatively in 24 hours. (Clark and Lane, 1961).

In both P. utriculus and P. physalis the gas in the float can be regulated through a siphon to control buoyancy. The gastrozooids are highly modified polyps with one large feeding tentacle that bears several cnidae. The feeding tentacle can reach lengths of up to ten meters in large Pacific exemplars. Dactylozooids also have one long, unbranched tentacle. Gonozooids produce sessile gonophores that are never released as free medusa (Brusca, Moore and Shuster, 2016). Various types of zooids bud in groups called cormidia at the base of the pneumatophore. Each cormidium acts as a colony-within-a-colony composed of a shieldlike bract, gastrozooids and one or more gonophores that may acts as swimming bells. The cormidia can break loose from the parent colony to live an independent existence, at which time they are termed eudoxids (Brusca, Moore and Shuster, 2016).

Siphonophore zooids (Adapted from Brusca, Moore and Shuster, 2016)

Cystonectans like P. utriculus possess an anterior gas-filled float or pneumatophore and a posterior, zooid-bearing siphosome (Brusca, Moore and Shuster, 2016). The following are the main characteristics of the zooids found in blue bottles:

Gastrozooids: basal mass of nematocyst batteries, epidermis (bearing nematocyst batteries), mouth, tentacle branched with tentilla.

Dactylozooids: long contractile tentacle (unbranched) where nematocysts are found. Nematocysts migrate from a basal cellular mass towards the tentacle and replace discharged nematocysts after feeding events.

Gonozooids: complex in structure, gonozooids produce both male and female gonophores, which remain attached to the zooid and a cluster of nematocyst batteries for defence.

 

Physalia utriculus Gold Coast, Australia (2019)

Certain species of nudibranchs have been observed to release mucus that is not detectable by the chemosensory structures of hydrozoans (e.g. the cnidocil) to envelop the tentacles of hydrozoans in order to feed on the intact, unfired nematocysts (Greenwood, 2009). Glaucus atlanticus (blue dragon), an aeolid nudibranch, is not only able to thwart the sensory system of siphonophores (e.g. Physalia sp.) and feed on their tentacles, but can also store nematocysts in their cerata. Nematocysts that are ingested, incorporated and used by G. atlanticus are referred to as kleptocnidae (“stolen cnidae”). Some aeolid nudibranchs such as blue dragons have evolved to have a hard chitin cuticle inside the digestive tract that confers them extra protection against the venomous tentacles of their prey (Greenwood, 2009).

One species of ctenophore, Haeckelia rubra, and certain turbellarians are also known for being able to prey upon and steal cnidocytes, not from siphonophores, but from narcomedusae.

Juveniles of the fish species Nomeus gronovii, the bluebottle-fish, hide and shelter amongst the tentacles of Physalia physalis. Other symbioses between Physalia sp. and pelagic species have been observed but are still poorly studied.

Blue bottles are suspension feeders, they capture and ingest zooplankton and small fish in the water column. Their diet can include fish eggs, larvae and fecal pellets. They can also prey upon small crustaceans and soft-bodied invertebrates while they feed close to the surface or in shallow waters. Some of the specimens that I collected had copepods entangled in their tentacles. The copepods were of a suitable size to be eaten by the blue bottles (~3 mm) and some of them displayed an unusual blue coloration indicating that they had been in contact with the tentacles. They also showed symptoms of hyperexcitability, swimming relentlessly and in an uncoordinated manner around the tanks, probably due to the neurotoxic effects of the venom.

Large populations of blue bottles can deplete small local fisheries and are believed to play important roles in pelagic ecosystems. The fact that blue bottles feed mainly on small zooplanckton suspended on the water column, on the lower levels of trophic chains, makes this species a good indicator of the stability of an ecosystem.

Known predators of hydrozoans are the leatherback sea turtle (Dermochelys coriacea), nudibranchs and ctenophores.

Hydrozoan polyps reproduce asexually by budding. The cell wall evaginates and incorporates a section of the gastrovascular cavity. The mouth and tentacles arise at the distal end and eventually the bud detaches from the parent polyp. In Physalia utriculus, the bud can remain attached to the rest of the colony until they are released along with a departing eudoxid (independent cormidium) (Brusca, Moore and Shuster, 2016).

Siphonophores can produce chains of individual medusa buds called cormidia, which can break free to begin a new colony. All hydrozoans cnidarians have a sexual phase in their life cycle (except for Hydra, where the sexual medusoid stage is absent). Siphonophores appear to be ancestrally gonochoristic but hermaphroditic forms exist among the Physonecta and exclusively among the Calycophorae (Codonophora) (Brusca, Moore and Shuster, 2016).

In Hydrozoa, cleavage during embryonic development is usually radial or holoblastic. A coleoblastula forms and then gastrulates into a steroagastrula with an endoderm and an ectoderm. The stereogastrula then elongates to form a planula larva, which is radially symmetrical. The endoderm becomes the gastrodermis and the ectodermis develops into the epidermis. The posterior end of the planula larva develops into the mouth. The larva undergoes a reorganization of the nervous system that gives rise to the primary polyp.

Some siphonophores undergo direct development without a larval stage (Brusca, Moore and Shuster, 2016). P. utriculus is gonochoristic, so the individual gonozooids within a single blue bottle are made up of either male or female gonophores. Fertilization occurs when gametes are released from the gonophores into the water column, which can happen simultaneously as gonozooids break free from the colony (Hammond, 2009).

Spawning is thought to be density-dependent and triggered by both chemical and light signalling, which could explain why Physalia populations have large proportions of juveniles during spring in the southern hemisphere. Gametes originate within the gonophore from a layer of germ cells separated from the coloenteron by a mesodermal layer of multinucleated cells called spadix. As the gonophore develops, germ cells mature into spermatogonia and oogonia of approximately the same size, but arranged into layers differently (clusters of cells and thin layers, respectively) (Hammond, 2009). Trace amounts of yolk can be found in the cytoplasm of oogonia.

Lisa-ann Gershwin, a marine invertebrate expert and author of Stung! (2013), suggests that the floats on blue bottles can lean either to the left or to the right, depending on the position of the cormidia underneath it. This is thought to be a natural mechanism to ensure that only a proportion of the population is blown onshore and stranded during certain wind conditions (Ennion, 2016). The aboral sail in Vellela resembles the pneumatophore in Physalia and is also used to sail at an angle to the wind, a similarity that is thought to be the result of convergent evolution. Blue bottles can use muscle contractions to modify the shape and size of the float, thus changing the direction of drift.

Cnidae in Cnidaria are produced by cnidoblasts, which develop from interstitial cells in the epidermis. The cnidoblast produces a large vacuole inside which a complex and poorly understood reorganization takes place. Once the cell is fully formed, the cell is termed cnidocyte, and includes a cnidocil for sensing, located next to the operculum (Brusca, Moore and Shuster, 2016), a capsule that contains the coiled tube and the stylets and spines for attachment and delivery of neurotoxins.

The tentacles of P. utriculus are contractile due to the existence of longitudinal and circular myofibrils derived from the ephitelium. Blue bottles also have the ability to transfer liquid across their gastrovascular cavity via contractions mediated by RFamides. the same biochemicals that cause cardiac contractions in higher metazoans (Yanagihara, 2002). For feeding, P. utriculus uses its cnidocytes to capture and paralyse its prey.

The mechanism by which the nematocysts are discharged during predation is called exocytosis, and it is still not fully understood. This is mainly due to the small size of cnidae and the high velocity at which tubules are fired by the nematocysts (2 m/s). However, there are three hypotheses (Brusca, Moore and Shuster, 2016) to explain the nature of the process. The osmotic hypothesis suggests that the protrusion of the tubule from the nematocyst capsule results from a sudden change in hydrostatic pressure inside the cell cause by a rapid influx of water. In the tension hypothesis, the force needed for the discharge of the tubule comes from the intrinsic tension generated during the formation of the cnidocyte. This tension is released during a predation event. The third hypothesis, the discharge results from contractile forces that squeeze the nematocyst and cause the protrusion of the tubule from the capsule.

It is not fully understood whether the blue coloration in P. utriculus serves any specific function, but is thought to protect them from UV radiation. The blue colour might also serve for aposematic purposes, to warn predators of their toxicity. It might also simply be that the venom happens to reflect light at that particular wavelength. Dr. Angel Yanagihara, from The University of Hawaii, suggests that the blue coloration could come from dinosterol (Yanagihara, 2002), a common steroid alcohol in dinoflagellates.

For this study, the specimens were fixed in 4% PFA for three weeks, and the specimens did not lose their blue coloration. However, For the DAPI fluorescence staining, the specimens had to be submerged in ethanol beforehand, this caused the blue pigmentation to be lost almost completely after several washes. This was an interesting outcome that could provide new insights on the biochemistry of these pigments. Blue bottles interact with their environment through specialized structures; statocysts allow them to detect gravity for orientation, cnidocils on nematocysts allow the cells to sense chemical and mechanical changes that trigger the release of the tubule from the capsule for predation and defence. Light stimuli are thought to be detected by clusters of nerves in the translucent parts of the zooids (Brusca, Moore and Shuster, 2016).

Blue bottles (Physalia utriculus) are often mistaken for Portuguese men-of-war (Physalia physalis). However, blue bottles are common in the Indo-Pacific, while P. physalis predominates in the Atlantic ocean. Due to the life cycle and lifespan of these species (about six weeks), it is unlikely that populations will be able to spread outside their natural range. Blue bottles float on the surface and drift with ocean currents (e.g. the East Australian Current) until strong wind conditions cause them to strand along the coastline.

Some biologists have hypothesized that the varying orientation of the float relative to the cormidium results in a natural mechanism that ensures that not all individuals end up on the same locations during strong wind regimes, improving the inter-population spread of genetic resources and the survival and evolution of the species.

The blue bottles collected for this study were found in Surfers Paradise beach (Gold Coast, Australia) and are likely to carry slightly different genetic information from their relatives on other parts of the Pacific (e.g. those found in Galápagos, Ecuador). In South America, the Atlantic cousins of blue bottles are particularly abundant along the northeast coast of Brazil, especially during summer months.

As far as phylogenetics goes, the evolutionary history of Physalia utriculus can be studied by looking at the evolution of the phylum it belongs to: Cnidaria. P. utriculus is a sister taxon of Physalia physalis, they are the two species in the genus Physalia. Physalia physalis is known as the Portuguese man o’ war and can grow larger than their Pacific cousins, with some individuals reaching up to 13 meters in length.

Phylum: Cnidaria

The phylum Cnidaria is a highly diverse group that includes jellyfish, sea anemones, corals and other less familiar forms such as siphonophores, zoanthids and myxozoans. There are three fundamental characteristics that define the species on this monophyletic taxon (Brusca, Moore and Shuster, 2016); the first is the possession of cnidae, which are tubular structures contained within cellular capsules and aid in prey capture, attachment, locomotion and defence. Second is the tendency to form colonies by asexual reproduction. And third is the existence of a dimorphic life cycle, usually characterised by polypoid and medusoid forms. The unique polyp form of Cnidaria, their planula larvae and their cnidae are three of the synapomorphies that define this phylum. Cnidarians are diploblastic, possess radial or biradial symmetry, an incomplete gastrovascular cavity and a middle layer called mesenchyme or mesoglea (Pontin and Cruickshank, 2012), which can be composed of both non-cellular and cellular components, although some species have non-cellular mesoglea only.

According to Dr. Angel Yanagihara from the University of Hawaii, the main trait that defines the monoplhyly of siphonophores is the high complexity of colony structure. In the same study, Yanagihara and her team were able to study the phylogenetic relationships within the clade Hydroidolina, using mtDNA from 26 representative species within this clade, including the siphonophores Physalia physalis and Nanomia bijuga. They used 19 non-hydrozoan taxa as outgroup for this tudy. They concluded that Siphonophorea was the first taxon to evolve divergently from the Hydroidolina clade (Kayal et al., 2015).

Researchers from The University of Queensland are currently working on a project to sequence the genome of Physalia utriculus, a work that will be useful to understand at a greater depth the autopomorphies that gave rise to the Physaliidae family, and to reconstruct more accurate evolutionary relationships between blue bottles and other hydrozoans. Sequencing the genome of this species will allow bioinformaticians to study homologies by comparison against known databases of other organisms, at the level of DNA (e.g single nucleotide polymorphisms or genome-wide associations). Yanagihara et al. suggested that, for now, researchers could benefit from using mitchondrial genomes instead of nuclear genomes because of the small size, the fact that it is highly-conserved and because of the low cost of sequencing such mitogenomes.

Due to the poor information on the conservation status of Physalia utriculus, the following section is largely based on rational (though not necessarily accurate) inferences.

The International Union for the Conservation of Nature (IUCN) does not have a conservation status for Physalis utriculus. In fact, the conservation status of most species of hydrozoans is unknown, mainly due to the cryptic nature of some of them and their complex life cycles, which makes it challenging to estimate the population structure, size and stability. However, it is sensible to infer that armadas of blue bottles can be affected by changes in temperature on the sea surface (SST).

Blue bottles employ an opportunistic (r-selected) life strategy and have no major predators, except for aeolid nudibranchs like Glaucus atlanticus and some species of turtles such as leatherback turtles (Eritmochelys coriacea). This means that the population size is regulated mainly by environmental factors such as the availability of nutrients, which will determine the abundance of planktonic food sources in the water column. It also means that population numbers can be affected by pollution or sediment runoff from waterways. 

Blooms can probably occur due to human activities or as a result of seasonal variability. P. utriculus has a delicate body architecture and several of its biological functions are density-dependent, so it is likely vulnerable to natural stresses such as storm surges, strong surface currents and oceanic gyres.

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