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Aplysina Cauliformis Classification Essay

original description (ofLuffaria elongoreticulata Carter, 1882) Carter, H.J. (1882). Some Sponges from the West Indies and Acapulco in the Liverpool Free Museum described, with general and classificatory Remarks. Annals and Magazine of Natural History. (5) 9(52): 266-301,346-368, pls XI-XII. [details]   

original description (ofLuffaria rufa Carter, 1882) Carter, H.J. (1882). Some Sponges from the West Indies and Acapulco in the Liverpool Free Museum described, with general and classificatory Remarks. Annals and Magazine of Natural History. (5) 9(52): 266-301,346-368, pls XI-XII. [details]   

original description (ofLuffaria cauliformis Carter, 1882) Carter, H.J. (1882). Some Sponges from the West Indies and Acapulco in the Liverpool Free Museum described, with general and classificatory Remarks. Annals and Magazine of Natural History. (5) 9(52): 266-301,346-368, pls XI-XII. [details]   

original description (ofLuffaria cauliformis var. rufa Carter, 1882) Carter, H.J. (1882). Some Sponges from the West Indies and Acapulco in the Liverpool Free Museum described, with general and classificatory Remarks. Annals and Magazine of Natural History. (5) 9(52): 266-301,346-368, pls XI-XII. [details]   

original description (ofLuffaria cauliformis var. elongoreticulata Carter, 1882) Carter, H.J. (1882). Some Sponges from the West Indies and Acapulco in the Liverpool Free Museum described, with general and classificatory Remarks. Annals and Magazine of Natural History. (5) 9(52): 266-301,346-368, pls XI-XII. [details]   

original description (ofVerongia longissima sensu de Laubenfels, 1936) Laubenfels, M.W. de. (1936). A Discussion of the Sponge Fauna of the Dry Tortugas in Particular and the West Indies in General, with Material for a Revision of the Families and Orders of the Porifera. Carnegie Institute of Washington Publication. 467 (Tortugas Laboratory Paper 30) 1-225, pls 1-22.
page(s): 23-24; pl 5 fig 2 [details]  Available for editors   [request] 

basis of record Wiedenmayer, F. (1977). Shallow-water sponges of the western Bahamas. Experientia Supplementum. 28: 1-287, pls 1-43.
page(s): 68-69 [details]  Available for editors   [request] 

additional source Zea, S. (1987). Esponjas del Caribe Colombiano. (Catálogo Cientifico: Bogotá, Colombia): 1-286.
page(s): 57-59 [details]   

additional source Díaz, M.C. (2005). Common sponges from shallow marine habitats from Bocas del Toro region, Panama. Caribbean Journal of Science. 41(3): 465-475. (look up in IMIS)
page(s): 468 [details]  Available for editors   [request] 

additional source Pinheiro, U.S.; Hajdu, E.; Custodio, M.R. (2007). Aplysina Nardo (Porifera, Verongida, Aplysinidae) from the Brazilian coast with description of eight new species. Zootaxa. 1609: 1-51.
page(s): 8-10 [details]  Available for editors   [request] 

additional source Van Soest, R.W.M. (1981). A checklist of the Curaçao sponges (Porifera Demospongiae) including a pictorial key to the more common reef-forms. Verslagen en Technische Gegevens Instituut voor Taxonomische Zoölogie (Zoölogisch Museum) Universiteit van Amsterdam. 31: 1-39.
page(s): 26 [details]   

additional source Muricy, G.; Lopes, D.A.; Hajdu, E; Carvalho, M.S.; Moraes, F.C.; Klautau, M.; Menegola, C.; Pinheiro, U. (2011). Catalogue of Brazilian Porifera. Museu Nacional, Série Livros. 300 pp. [details]  Available for editors   [request] 

additional source Rützler, K.; Piantoni, C.; Van Soest, R.W.M.; Díaz, M.C. (2014). Diversity of sponges (Porifera) from cryptic habitats on the Belize barrier reef near Carrie Bow Cay. Zootaxa. 3805(1): 1-129., available online at
page(s): 97 [details]  Available for editors   [request] 

additional source Vacelet, J. (1990). Les spongiaires. in Le Monde Marin. (ed. Claude Bouchon) pp 16-33. La Grande Encyclopédie de la Caraïbe. Editions Caraïbes, Pointe à Pitre.
page(s): 30 [details]  Available for editors   [request] 

additional source Van Soest, R.W.M. (2017). Sponges of the Guyana Shelf. Zootaxa. 4217: 1-225., available online at
page(s): 15-16 [details]  Available for editors   [request] 

additional source Pérez, T. ; Díaz, M.C.; Ruiz, C.; Cóndor-Luján, B.; Klautau, M.; Hajdu, E.; Lôbo-Hajdu, G.; Zea, S.; Pomponi, S.A.; Thacker, R.W.; Carteron, S.; Tollu, G.; Pouget-Cuvelier, A.; Thélamon, P.; Marechal, J.-P.; Thomas, O.P.; Ereskovsky, A.E.; Vacelet, J.; Boury-Esnault, N. (2017). How a collaborative integrated taxonomic effort has trained new spongiologists and improved knowledge of Martinique Island (French Antilles, eastern Caribbean Sea) marine biodiversity. PLoS ONE. 12 (3): e0173859., available online at
page(s): 9 [details]   

additional source Lehnert, H.; van Soest, R.W.M. (1998). Shallow water sponges of Jamaica. Beaufortia. 48 (5): 71-103.
page(s): 98 [details]   

additional source Lendenfeld, R. von. (1889). A Monograph of the Horny Sponges. (Trübner and Co.: London): iii-iv, 1-936, pls 1-50. , available online at;view=1up;seq=1
page(s): 417 [details]   

additional source Van Soest, R.W.M. (1978). Marine sponges from Curaçao and other Caribbean localities. Part I. Keratosa. In: Hummelinck, P.W. & Van der Steen, L.J. (Eds), Uitgaven van de Natuurwetenschappelijke Studiekring voor Suriname en de Nederlandse Antillen. No. 94. Studies on the Fauna of Curaçao and other Caribbean Islands. 56 (179): 1–94.
page(s): 62-63; pl XI 1, XII 2 [details]   

additional source (ofVerongia longissima sensu de Laubenfels, 1936) Laubenfels, M.W. de. (1953). Sponges from the Gulf of Mexico. Bulletin of Marine Science of the Gulf and Caribbean. 2(3): 511-557.
page(s): 515 [details]   

additional source (ofVerongia cauliformis (Carter, 1882)) Collette, B.B.; Rützler, K. 1977. Reef fishes over sponge bottoms off the mouth of the Amazon River. Proceedings 3rd International Coral Reef Symposium Miami, Florida, U.S.A. pp. 305-310. [details]   

additional source (ofVerongia longissima sensu de Laubenfels, 1936) Hechtel, G.J. (1965). A systematic study of the Demospongiae of Port Royal, Jamaica. Bulletin of the Peabody Museum of Natural History. 20: 1-103.
page(s): 13-14 [details]   

basis of record (ofLuffaria cauliformis Carter, 1882) Wiedenmayer, F. (1977). Shallow-water sponges of the western Bahamas. Experientia Supplementum. 28: 1-287, pls 1-43. [details]  Available for editors   [request] 
 Present  Inaccurate  Introduced: alien 

From editor or global species database

Taxonomy Please note that this is based on Carter's Luffaria cauliformis (1882 p. 268). This is not Aplysina cauliformis Carter, 1882: 270, which is a Callyspongia. [details]

To Barcode of Life (8 barcodes) 
To Biodiversity Heritage Library (12 publications) 
To Biodiversity Heritage Library (2 publications) (from synonym Luffaria cauliformis Carter, 1882)
To Biodiversity Heritage Library (2 publications) (from synonym Verongia cauliformis (Carter, 1882))
To Biodiversity Heritage Library (5 publications) (from synonym Verongia longissima sensu de Laubenfels, 1936)
To Encyclopedia of Life 
To Global Biotic Interactions (GloBI) 
To Sponge Barcoding Database (Aplysina cauliformis) 
To Sponge Barcoding Database (Aplysina cauliformis) 
To Sponge Barcoding Database (Aplysina cauliformis) 
To Sponge Barcoding Database (Aplysina cauliformis) 
To Sponge Barcoding Database (Aplysina cauliformis) 
To Sponge Barcoding Database (Aplysina cauliformis) 
To USNM Invertebrate Zoology Porifera Collection (8 records) (from synonym Verongia longissima sensu de Laubenfels, 1936)

1. Introduction

Marine sponges have been known and used by mankind since antiquity. They were included in the first classification of living organisms, written in 350 BC by Aristotle in Greece. At first thought to be plants, their animal nature was only recognized by the end of the XVIII century. However, great naturalists of the time such as Lamarck, Linnaeus and Cuvier classified them as Zoophytes. The elevation of the Porifera to the level of phylum was suggested by Huxley in 1875 and by Sollas in 1884, and was only accepted at the beginning of the XX century [1].

Sponges belong to the phylum Porifera and are the most primitive of multicelled animals, having existed for roughly 700–800 million years. They have a very simple physiology of construction. They are aquatic organisms growing mostly in temperate salt waters but may also be found in fresh water. When reaching adult form, they are found in solid substrates in places that allow adequate conditions for their growth. Some, when in their primary states, may be mobile [2–4]. They are easily found in all marine environments, from the intertidal zones to the ocean depths of 8500 m in tropical and polar seas. Despite their wide distribution in terms of different oceans and depths, the rocky non-polluted coastline areas show greater populations of sponges which are also known for being rich in secondary metabolites [5–9].

The sponges are filtering animals, which utilize flagellate cells called coenocytes for promoting the circulation of the water through a system of canals existing in this phylum only called aquifer system, around which their body is built. This water flow brings organic particles and microorganisms which are filtered and eaten [10]. Of all the known sponges, only 1% grow in fresh water [11].

There are basically three classes of sponges, Calcarea (5 orders and 24 families), Desmospongiae (15 orders and 92 families) and Hexactinellida (6 orders and 20 families). So far, about 15,000 species of sponges have been described, their diversity however is believed to be much bigger than this [4,12]. Being sessile simple organisms, they evolved chemical defense mechanisms to protect themselves against predators and competitors, as well as against infectious microorganisms. Studies show that secondary metabolites in sponges carry out a crucial role in their survival in the marine ecosystem [13,14].

Because of their potential for the production of new substances of pharmacological interest, sponges have been one of the most chemically studied organisms. In the past 20 years, hundreds of substances have been isolated from them and many of those substances have already been identified, and present interesting biological and pharmacological (such as antibacterial, anticoagulant, antifungal, antimalarial, antituberculosis, antiviral, immunosuppressive and neuro-suppressor) activities [15–23]. The main reported activities for the Aplysina genus are antibacterial, antiyeast, antifungal, antiviral, cytotoxic and hyperglycemic activities, which can be seen in Table 1.

The pioneer investigative work in the field of sponge chemistry published by Bergmann and Feeney in the beginning of the 1950s led to the discovery of Cryptotethya crypta bioactive nucleosides spongothymidine and spongouridine [21]. These nucleosides were the basis for the synthesis of Ara-C, the first marine derivative anticancer agent, and antiviral drug Ara-A [22]. Today, Ara-C is used in the routine treatment of patients suffering from leukemia and lymphomas. One of its derivatives was also approved for use in patients with cancer of the pancreas, lungs and breast [23].

The Genus Aplysina

The genus Aplysina, formerly known as Verongia and reclassified to Aplysina, is one of the richest in terms of secondary metabolites, described in 14 species of the family Aplysinidae, there are 2 species from the Mediterranean Sea, 8 from the Caribbean, 3 from the Pacific Coast of Mexico and 15 in the Brazilian coast. Of the above species, 8 have only been recently identified. From the Mediterranean Sea, the two described species of the genus Aplysina are: A. aerophoba (Schmidt, 1862) and A. cavernicola (Vacelet, 1959). From the Caribbean, among others we find A. fistularis insularis, A. fistularis form fulva, A. archeri, A. cauliformis and A. Lacunosa [33].

Like other genera of the order Verongida, Aplysina stands out for its unique biochemical characteristics. They show low terpene content, and possess a moderately high percentage of sterols, mostly within the aplystan skeleton. They also produce a significant series of brominated derivatives of tyrosine metabolites considered peculiar to species of this order. The sponges of this order are also known for their high phenotypic variability [34].

Marine organisms produce a cocktail of halogenated metabolites with potential commercial value. The structures found in these compounds go from linear chain acyclic, to complex polycyclic molecules [35,36]. The research of halogenated metabolites has been more focused on marine algae than on sea sponges [37–41]. Though many compounds have been discovered recently, many sponges species are poorly screened and the need for new drugs keeps this field open.

In a previous paper our research group evaluated crude algae, sponge extracts and chemically determined molecules from Northeastern Brazil [42–48] with database survey [49–62].

In this paper we review halogenated substances from the genus Aplysina. A compilation of the 13C NMR spectral data of the selected natural products is also provided. This type of genus and species investigation is helpful in the identification and capture of halogenated substances from the genus.

2. Methodology

An extensive bibliographic review was carried out to identify studies of halogenated substances isolated from the genus Aplysina. The present review covers the period of 1967 thru 2010. The search was performed using the following databases: NAPRALERT (Natural Products Alert at the University of Illinois, Chicago), Chemical Abstracts, and the Brazilian online scientific literature search system called “Periodical CAPES” (Coordination for the Improvement of Graduate Level Personnel).

Tables 2 and 3 respectively show the halogenated substance distribution in the genus Aplysina, and the basic skeletons of those substances. Table 4 shows the different substituents for the diverse classes of halogenated substances. Table 5 describes the position of the substituents for the 101 substances isolated from each species. Finally Tables 6–14 show a compilation of 13C NMR data of the substances.

Although the isoxazoline alkaloids are the group with more 13C NMR data, some chiral centers of this group continue with an undefined stereochemistry due to the incompatibility of using X-ray crystallography techniques, possessing sometimes non-crystalline characteristic [98]. Some positions with 13C NMR data had to be revised because there were mistakes in the numbering of the carbon skeleton in the attribution of values of some positions in this group of alkaloids.

3. Discussion

The genus Aplysina belongs to the order Verongida, sponges with a wide variety of metabolites. Sterols [110,111], carotenoids [112], amino acids [113] and rare fatty acids [114] have all been isolated from this order. However, the peculiarity of this order is from the ecological and medicinal points of view, in that great production of halogenated substances originates from the metabolism of amino acids such as phenylalanine and tyrosine. The halogenated substances found in the marine sponges of the genus Aplysina can be classified as: (A) Bromotyramines, (B) Cavernicolins, (C) Hydroverongiaquinols, (D) Bromotyrosineketals, (E) Bromotyrosine lactone derivatives, (F) Oxazolidones, (G) Spiroisoxazolines, (H) Verongiabenzenoids, (I) Verongiaquinols and (J) Dibromociclohexadiens.

3.1. Chemotaxonomy Importance of Aplysina Sponges

Although in the past, it was suspected that bromotyrosine compounds were not present in Brazilian Aplysina species [69], nowadays numerous studies have shown the presence of these chemical biomarkers, not only in Brazilian species, but in almost all the Verongida order.

In order to classify the large number of halogenated compounds reviewed in Table 2, for each sponge species, we listed the halogenated compounds under the correlated species. Considering the taxonomic species diagnosis of morphologic variation of spongin fibers is difficult [33], chemical composition can be used as a tool for a more accurate identification. The distribution of the halogenated compounds is widespread in Aplysina genre, and studies show that mainly bromoisoxazoline alkaloids have been found in almost all species. This family of metabolites was usefully employed as a chemical marker for the distinction of some taxa as Aplysina aerophoba and Aplysina cavernicola, two very physically similar species [63], but biochemically different. In another situation, majority of aerothionine was key to identify two subspecies of A. fistularis, which split into A. fulva and A. insularis [115].

The similarity between agelorins A and B, isolated from Agelas oroides and produced by Aplysina caissara, was essential to show the two genera, Aplysina and Agelas, have a phylogenetic relationship [76] and 11-epi-fistularin-3 was yielded by Aplysina fulva [98].

The presence of stereo metabolites isolated from Aplysina sponges as derivatives of fistularin-3 discussed by Rogers et al., 2005 [98], provides evidence that enzymatic pathways are non-stereoselective in these sponges.

As can be seen, each kind of genus adds a different profile of metabolites. However, even with a different chemical profile, Aplysina sp. has compounds that give a clue to their evolutionary origin.

3.2. Bromotyramines

The substances aplyzanzine A, aplysamine-1 and aplysamine-2 present a dibromotyramine structural portion, and probably originated in accordance with Evan et al. [82], by amidation with other bromotyrosinated radicals. Moloka’inamine [116] and purealidin C isolated from Psammaplysilla purea [90] are examples of metabolites isolated from sponges of the order Verongida, having dibromotyramine in their structures. According to Carney, free phenolic groups are important precursors nitrile phenolic [96], hence the similarity between methoxylated compound, aplysamine-2, and hydroxylated analogue, psammaplin-A [84], observed by Xynas and Capon, 1989, shows that psammaplin-A may be important precursor aplysimines as much of the fistularin and its derivatives

3.3. Cavernicolins

Cavernicolines are γ and δ-lactames formed by a residual halogenated tyrosine precursor [81] and also having a bi-cyclic system. The junction of the rings occurs in carbons C-3 and C-4 in ortho position, while in the 7-bromocavernicolenone and in the 7-chlorocavernicolenone, this junction occurs in carbons C-2 and C-4. They can be defined as haloperoxidases with the role of converting either the 3-chloro (V) ortho 3-bromotyrosine (IV) in residues of 3,5-dichloro (VIII) or 3,5-dibromotyrosine (VI) or 3-chloro-5-bromotyrosine (VII) or 3-bromo-5-chlorotyrosine (IX), respectively [80]. These substances have a chiral center at C-2 and their R and S enantiomers are obtained in racemic mixtures, or relatively pure from the genus Aplysina. In the formation of cavernicolines, as to the substitution pattern (ortho or para) it is suggested that the biosynthesis pathway has either a halotyrosine (XV, XVI, XVIII and XVIX) or a halo-dopa (XIV and XVVI) intermediary which will form a spirolactone precursor (XXII and XXIII), allowing the formation of intermediaries in racemic or quasi-racemic mixtures. The absence of control in the absolute stereochemistry of this class is intrinsic to phenol oxidative coupling [81,117]. It is noteworthy that experimental observations [118] show that 3,5-dibromo-4-methoxyphenylalanine methyl ester (XX) in reaction in an anodic oxidative medium form a more appropriate intermediary (XXI) than the spirolactone, originating derivatives similar to the stereoisomers of the cavernicolines with considerable yields (See Figure 1).

3.4. Hydroverongiaquinols

The hydroverongiaquinols are 2,6-bromotyrosine phenolic derivatives. Both the hydroverongiaquinols and the verongiabenzenoids are important mediators in biosynthesis of other classes of bromotyrosine metabolites. The verongiabenzenoids are part of the biosynthesis of isoxazoline alkaloids, and hydroverongiaquinols are important precursors in the formation of metabolites which need free phenolic groups to convert themselves into α-oximine substances, such as the phenolic nitriles. However, phenolic nitriles have not been found in the genus Aplysina, they are found in the genus Ianthella where substances like the bastadins, are important chemotaxonomic markers for the genus [119].

3.5. Bromotyrosineketals

The bromotyrosineketals have a 3,5-dibromocyclohexa-2,5-dienyl ketal skeleton system. Literature shows that the dimethoxy and methoxy-ethoxy ketals (XXXII