Drupella+rugosa

The Coral-eating snail Rugose Drupe //Drupella rugosa// (Born, 1778) Figure 1. //Drupella rugosa.// Image by Wu Meng Yue. = Introduction =

toc //Drupella rugosa// (Family: Muricidae) is a species of marine snail of a genus that is known as a ‘silent killer’ of coral reefs 1]. Corallivory is the consumption of live coral tissue, skeleton, mucus and larvae and //D. rugosa// is a known corallivorous organism 2].

//Drupella// snails are capable of having a similar, if not greater, impact on coral reefs than another well-known corallivore, the crown-of-thorns sea star when present in large numbers and //D. rugosa// is no exception 3,4]. It is astonishing that a small marine snail that can reach up to 4 cm in length is capable of match the destruction done by large crown of thorns sea star that are generally 25 cm in diameter.

= Environmental impact =

Corallivory plays a role in maintaining ecosystem balance 5]. Similar to //D. rugosa,// Crown-of-thorn sea star is a corallivore with a preference for branching corals. Scientist have hypothesised that this sea star may a play a role in preventing the dominance of fast growing branching coral genera in reefs by their feeding 6]. //Drupella rugosa// may also play a similar role, but the impact of //Drupella// is not always positive.

Climate change and humans
Climate change and anthropogenic influences are believed to further exacerbate the negative impacts. Global warming and ocean acidification can act as stressors to the corals. //Drupella rugosa// had been found to prefers corals that are experiencing mechanical or environmental stressors as they may have impaired or non-functioning nematocysts 7, 8].

The increase in temperature may also increase the feeding rate of //D. cornus// as well 9], whether this trend is found in //D. rugosa// is still not known. Nutrient run off from human activities can also promote the growth of //Drupella// juveniles 10]. Both may help increase //Drupella// population on the reef. With Singapore temperature rising at double the global average 33], the impact of //Drupella// on our local reefs needs to be addressed.

Population growth
In the last 20 years, //D. rugosa// population 'outbreak' in the Indo-Pacific region had been noted 11]. Population outbreak is defined as “any population of elevated density (> 2 individuals/sqm) that causes extensive mortality of corals and persists for months or years over large areas of reef” 7]. Recently, an argument was put forward to determine the difference between 'population outbreak' and 'seasonal feeding aggregation' 12].

Even so, it is known that large population of //Drupella// can cause mass coral mortality. For example, population growth of //D. rugosa// and //D. margariticola// had caused more than 60% coral death in Hong Kong and Thailand 13,14]. This may cause a lost in coral diversity due to their feeding preference.

Thankfully, there is no evidence of a 'plague-like' population growth of //Drupella// since 1999 12]. But as our climate continues change, the situation may not stand true. Figure 2. Large aggregation of Drupella under a free-living coral. Persistent aggregation may lead to what scientist term a 'population outbreak'. Image by Christopher D. Wells, used under [|CC BY-NC-SA 2.0].

Dying corals?
Coral reefs are one of the most diverse and threaten ecosystem on earth. Hence, a lot of money and manpower have been given to help conserved the reefs. To restore degraded reefs, restoration methods like coral nurseries and transplantations had been widely implemented and are essential to reef restoration methods.

Coral transplants are usually fast growing branching corals that are fragmented into smaller pieces, making them susceptible to //Drupella// predation 15]. This can be seen in Kenya, Red sea and Hong Kong where //Drupella// was found to be causing coral mortality in the transplants 16,17,18]. //Drupella rugosa// is also found munching on our local reefs and nurseries.

//Drupella// are well camouflaged by the calcareous algae and tend to hide in between the coral branches making removal of //Drupella// difficult and labour intensive. Caution is also needed during removal when reaching into the branches of the corals where the snails are at to ensure minimal damage to the coral itself. With their ability to attract conspecifics, constant inspections have to be done to reduce coral mortality 17].

Together with the fact that //Drupella// population can reach very high levels, manual removal of the snails can be labour intensive. In Thailand, volunteers had removed almost 14,000 //Drupella// in 2016 alone! 19] Figure 3. Removal of //Drupella cornus// from coral transplant. Tweezers had to be used to carefully retrieved the snail out of the coral to prevent further damage to the coral. Image by Shafir //et al.// (2010). In Singapore, manual removal of //Drupella// is also employed since a better method had not been found. The team in Koh Tao, Thailand had tried to create a '//Drupella// Dredger' to vacuum up the snails via crowdfunding, however the project was not successful. This may imply that more awareness on the impact of //Drupella// predation is needed to come out with more effective mitigation methods.

Figure 4. Screenshot of the crowdfunding page for the //Drupella// Dredger, here. Image by Wu Meng Yue. = Biology =

Adaptations to corallivory
//Drupella rugosa// is known as an obligate corallivore, this means that live coral polyps are an essential part of its diet. Nematocysts, zooxanthellae and mucus from corals was found in its stomach content 20]. It was also found to generally only consume the coenechyme of the corals 12].

As an obligate corallivore, //D. rugosa// possesses a specialised radula, with extremely long lateral teeth, to remove coral polyps and leave behind the white coral skeleton 3]. The radula is unlike any other muricids, including the other corallivorous subfamily coralliophilinae from the same family 21]. Interestingly, corallivorous organisms are only found in Coralliophilinae in Muricidae with // Drupella // (Subfamily: Ergalataxinae) being the exception, signifying multiple independent acquisition of corallivory in Muricidae 22].

Other adaptations include an external cuticularised proboscis that acts as a shield for the vulnerable tissues from the coral nematocysts 22]. An external proboscis also allows the snail to feed on adjacent live polyps while immobile 23]. Figure 5. White scar on //Pocillipora damicornis// from predation by //Drupella rugosa.// Image by Daryl David Ho & Wu Meng Yue.

Feeding behaviour
//Drupella rugosa// commonly feeds in groups (<20 individuals) because the feeding of an individual can attract other conspecifics 24]. This phenomena is hypothesised to be for protection and improve feeding efficiency 7]. Large feeding aggregation (~2000 individuals) is also known to occur and these aggregation tends to stay upon the prey coral colony for a longer period of time causing more damage to the reef 12]. These groups and aggregation may have more than one species of //Drupella//, and it will usually contain //D. rugosa// 7]. They are usually nocturnal feeders, but may feed during the day when present in sufficiently large numbers 4]. Figure 6. Feeding aggregation of //Drupella//. Image by John Turnbull, used under [|CC BY-NC-SA 2.0]. // Drupella rugosa // exhibits a preference for particular type of corals. The snails prefer branching corals such as //Acropora, Montipora// 4]//,// and in Singapore reefs, //Pocillipora//. This does not mean that other coral species are safe from //D. rugosa// predation because they are capable of shifting their dietary preference to other coral species 13].

Reproduction
// Drupella rugosa e // gg capsules can be found on recently consumed corals 25]. The coral skeleton exposed from feeding can act as a hard substrate for egg-capsule attachment 3, 25]. As they prefer branching corals, the egg capsules are found between the branches offering protection from predators and water currents 3] (Figure 7). The adults then move on to another coral colony to feed 13]. Figure 7. Egg capsules of //Drupella rugosa// on the branches of //Pocilopora damicornis// as indicated by the red arrows. Image edited from Sam //et al.// (2017) by Wu Meng Yue. Billiform (blister-shaped) eggs capsules are attached to the coral skeleton by a wide flatten base. Each female deposited an average of 52 capsules with a mean of 67 embryos per capsule. Hence, one //D. rugosa// is capable of producing 3484 embryos per spawning event. The latest understanding of the life cycle of //D. rugosa// is summarised below.

Figure 8. Life cycle of //Drupella rugosa//. Freshly-laid egg capsules are cream in colour, and become brown when the embryos are developed. Veliger larvae are release 15 days post-oviposition and stays near water surface or in the water column. Duration of the planktonic phase is not known to science yet. Image was created based on Sam //et al.// (2017) by Wu Meng Yue. A free swimming veliger larvae is hatched from the capsules allowing for dispersal of juveniles by ocean currents. //Drupella// larvae can also attract conspecifics resulting in large //Drupella// population on the reef. More individuals may cause more egg capsules to be laid, more larvae to survive to adulthood resulting in an increase in //Drupella// population on a reef. This could be the biological cause of //Drupella// outbreak on reefs 8].
 * media type="file" key="S1.m4v" width="300" height="300" || media type="file" key="S2.m4v" width="300" height="300" || media type="file" key="S3.m4v" width="300" height="300" ||
 * Video 1. Pre-hatching veligers developed transparent shell and visceral mass and yolk. They move slowly within the confines of the still cream coloured egg capsules. Video extracted from //Sam et al. 2017//, used with permission. || Video 2. Closed to hatching, egg capsule becomes brown and pre-hatching veligers becomes more mobile. Video extracted from Sam //et al.// 2017, used with permission. || Video 3. Veliger of //Drupella rugosa// as it swims in the water column. Video extracted from Sam //et al.//, 2017, used with permission. ||

Habitat
//Drupella rugosa// is usually found in sheltered reef environments, hidden within the corals 4]. There were also records of //D. rugosa// found in the eulittoral zone and shallow rocky shores 26].

= Distribution =

//Drupella rugosa// is found in the Indo-Pacific reefs, specifically, East Africa, Southeast and Northeast Asia. Figure 9. Distribution map of //Drupella rugosa// based on occurrence records available in GBIF database. In total, there are 360 georeference records available. Image extracted from Global Biodiversity Information Facility (GBIF), accessed 27 Sep. 2017. In Singapore, //D. rugosa// can be found in the fringing reefs of Kusu and Lazarus Island.

= Description =

Figure 10. Shell morphology of //Drupella rugosa//. The white arrow refer to the teeth on the outer lip and the red arrow refers to the plaits on the columella. Image edited from Rebecca Loh by Wu Meng Yue. || Description of //D. rugosa// given by Richmond (1997) 26] and Döring (2015) 27]: Figure 11. Soft body of //Drupella rugosa.// Image by Wu Meng Yue. || * Soft body is green with black spots Figure 12. Diagram of radula. Image extracted and adapted by Wu Meng Yue, used under CC BY-SA 3.0. Image from WikiCommons. || * Extremely long lateral teeth || = Diagnosis =
 * [[image:Drupella1.jpg align="center"]]
 * Shell length can reach up to 4cm
 * A moderately high spire
 * Body whorl contain five spiral rows of prominent tubercles (a round projection) separated by 12 axial ribs with fine granules
 * The nodules in the upper whorls gives an overall knobby appearance
 * The outer lip have 5-6 teeth
 * Protruding plaits on the columella
 * Elliptical aperture ||
 * [[image:Soft body.jpg width="400" height="259" align="center"]]
 * Cuticularised proboscis can sometimes be seen between the tentacles ||
 * [[image:radula.jpg width="400" height="200" align="center"]]

There are two known species of //Drupella// in Singapore – //D. rugosa and D. margariticola// and they tend to be found together. The two species have similar morphology (green soft body, bumpy columella, similar shell size and presence of nodules) with a couple of differences listed below. Image by Astri Noorbaini Binte Samsuri, used with permission. || **// Drupella margariticola //** Image by Astri Noorbaini Binte Samsuri, used with permission. || //Drupella// are notorious for being hard to identify in field due to the growth of pink calcareous algae on their shells 4], obscuring the morphology of their shells. Figure 13. Calcareous algae growth on the shell of //Drupella//, obscuring the distinguishing shell morphology. Image extracted by Wu Meng Yue, used under CC BY-SA 3.0. Image from WikiCommons. //Drupella// species look similar to other muricid drill snails (eg. //Thais//, //Morula//) 4,28] and tend to be misidentified without careful examination. This is a common mistake, even by taxonomists whom had erroneously placed this species into those genera due to similar morphology. An easy way to identify //Drupella// is the location of the snail. //Drupella// are usually found on or near corals because they are obligate corallivores, using corals for both food and shelter, while other genus of drill snails can be easily found on our rocky shores.
 * ** Distinguishing features ** || **// Drupella rugosa //** [[image:D rugosa.jpg width="400" height="220"]]
 * ** Shell morphology ** || Knoddy nodules  ||  Parallel ridges  ||
 * ** Aperture ** || White elliptical aperture  ||  Purple elliptical aperture  ||

= Taxonomy and Systematics =

Nomenclature
Binomial name: //Drupella rugosa// (Born, 1778)

Original combination: //Murex rugosus// Born, 1778 29] Original combination had been given erroneously as //Murex rugosa// in many online databases

Synonyms:
 * //Drupa concatenata// (Lamarck, 1822)
 * //Drupella concatenata// (Lamarck, 1822)
 * //Morula concatenata// (Lamarck, 1822)
 * //Murex concatenata// Lamarck, 1822 (synonym)
 * //Murex rugosus// Born, 1778
 * //Purpura alveolata// Reeve, 1846 (synonym)
 * //Purpura subturrita// Blainville, 1832 (synonym)
 * //Ricinula concatenata// (Lamarck, 1822)
 * //Thais alveolata// (Reeve, 1846)
 * //Thais rugosa// (Born, 1778)

Vernacular name: Rugose Drupe

Original species description
//Drupella rugosa// was first described by Ignaz von Born in 1778, under the name //Murex rugosus// in //Index rerum naturalium Musei Caesarei Vindobonensis// 29]. '//Rugosus//', meaning 'Roughened', may have been given to this species due to the presence of numerous tubercle found on the shell. Figure 14. Original description of //Drupella rugosa// (page 303) in Born (1778). Image extracted by Wu Meng Yue. Image from the Biodiversity Heritage Library. In 1925, Thiele placed this species into a new genus //Drupella// because of its corallivory behaviour and apomophies of its radula 22].

With the introduction of the International Code of Zoological Nomenclature, //rugosus// was changed to //rugosa// under the 'gender agreement'. The agreement states that the species name should follow the gender of the genus, thus the masculine '//rugosus//' was changed to the feminine '//rugosa//'. This led to the modern name of //Drupella rugosa//.

Type specimen
A syntype for //Purpura alveolata// Reeve, 1846, now a synonym of //D. rugosa//, can be found at the National History Museum, London labelled as NHMUK ZOO 1993131 of unknown locality 30,31].

Phylogeny
Taxonomy of the genus //Drupella// has be unclear, the genus had suffered excessive splits up to 12 species due to considerable morphological difference present 32]. The latest genetic study of the genus //Drupella// have five species and are classified under the family Ergalataxinae from the previous Rapaninae 22]. Species delimitation in that study had corresponded to the morphological species description, with the exception of //D. margariticola//, even though the nodes within //Drupella// are not well resolved (Figure 15) 22].

In the study, Bayesian analysis was carried out using 28S, 12S and cytochrome oxidase I (COI). Ribosomal genes (28S, 12S) were aligned using ClustalX while mitochondria gene (COI) was aligned by eye. MrModelTest is then use to find the best nucleotide substitution models for each gene partition out of 24.

A MrBayes bayesian phylogeny was created using concatenated analysis of all three genes sequenced and BEAST/GMYC was used to delimitate species. B oth MrBayes and BEAST analysis supports six //Drupella// species with a support value of 100 for all and //Drupella// being a monophyletic group (Figure 15). Yet, l ooking at the support values on the internal nodes of the tree, the values are quite low with one exception to // D. margariticola // 'Continental' (Figure 15). In conclusion, while the study support the monophyly of six //Drupella// species, the evolutionary relationship of this genus is still unclear.

With that conclusion, I believe the authors were using the phylogenetic species concept //sensu// Mishler and Theriot. Sadly, //D. minuta//, accepted by some authors, was not sampled and sequenced in this study. Whether this species is a valid species under this species concept is still not known. Figure 15. MrBayes phylogeny of //Drupella,// based on concatenated analysis of 28S, 12S and cytochrome c oxidase subunit I (COI). Support values are from MrBayes (above) and BEAST (BEAST) posterior probabilities given in percentage. Each grey box contain all specimens that GMYC had considered a species, specimen codes present in each box were removed for clarity. The root of this edited tree leads to other muricid outgroups. Image adapted from Claremont //et al.// (2011) by Wu Meng Yue. A Species Tree Ancestral Reconstruction was also carried out in BEAST assuming a relaxed lognormal molecular clock. It had been found that // Drupella // diversified approximately 5.0 Ma (Figure 13) and this correspond to the previous estimate previously based on morphology 22]. Figure 16. BEAST phylogeny of //Drupella//, based on combined analysis of 28S, 12S and cytochrome c oxidase subunit I (COI). Support values are BEAST posterior probabilities.The root of this edited tree leads to other muricid outgroups. Image adapted from Claremont //et al.// (2011) by Wu Meng Yue. With this result, corallivory in //Drupella// is found to be connected to the expansion and reorganisation of coral reefs in the Miocene unlike other corallivores that obtained this trait in the Oligocene with the major appearance of major coral groups 22]. //Drupella// is also a monophyletic group (Figure 16).

Classification
From the latest study, the classification of //D. rugosa// is given below:
 * Kingdom || Animalia ||
 * Phylum || Mollusca ||
 * Class || Gastropoda ||
 * Subclass || Caenogastropoda ||
 * Order || Neogastropoda ||
 * Superfamily || Muricoidea ||
 * Family || Muricidae ||
 * Subfamily || Ergalataxinae ||
 * Genus || // Drupella // ||
 * Species || // rugosa // ||

= Glossary =

Nematocysts: Specialised stinging cells of corals that act as organs for offence and defence. Zooxanthellae: Single-celled photosynthetic organisms that are able to live in symbiosis with corals, providing corals with food. Coenechyme: Coenechyme is the common tissue that surrounds and links the polyps in some corals. Proboscis: An elongated appendage on the head of the snail that is used for feeding. Apomorphy: A derived character trait that is distinct to a particular group of organisms.

= Acknowledgement =

I would like to thank Mr Tan Siong Kiat and Mr Daisuke Taira, without whom, this species page would not been possible.

= References =

[1] Boucher, L. M. (1986). Coral predation by muricid gastropods of the genus //Drupella// at Enewetak, Marshall Islands. //Bulletin of marine science, 38//(1), 9-11.

[2] Rotjan, R. D., & Lewis, S. M. (2008). Impact of coral predators on coral reefs. //Marine Ecology Progress Series, 367//, 73-91. doi: 10.3354/meps07531

[3] Turner, S. J. (1994). The biology and population outbreaks of the corallivorous gastropod //Drupella// on Indo-Pacific reefs. Oceanography and Marine Biology: An Annual Review, 32.

[4] Cumming, R. L. (2009). Case Study: Impact of //Drupella// spp. on reef-builging corals of the Great Barrier Reef. Great Barrier Reef Marine Park Authority.

[5] Rotjan, R. D., & Lewis, S. M. (2008). Impact of coral predators on coral reefs. //Marine Ecology Progress Series, 367//, 73-91. doi: 10.3354/meps07531

[6] Enochs, I. C., & Glynn, P. W. (2017). Corallivory in the eastern Pacific. In //Coral Reefs of the Eastern Tropical Pacific// (pp. 315-337). Springer Netherlands.

[ 7] Cumming, R. L. (2009). Population outbreaks and large aggregations of Drupella on the Great Barrier Reef.

[ 8] Cumming, R. L. (1999). Predation on reef-building corals: multiscale variation in the density of three corallivorous gastropods, Drupella spp. // Coral Reefs, 18 // (2), 147-157.

[9] Al-Horani, F., Hamdi, M., & Al-Rousan, S. (2011). Prey selection and feeding rates of Drupellacornus (Gastropoda: Muricidae) on corals from the Jordanian Coast of the Gulf of Aqaba, Red Sea.Jordan Journal Of Biological Sciences, 4(4),191-198

[10] Brodie, J., Fabricius, K., De’ath, G., & Okaji, K. (2005). Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence. Marine pollution bulletin, 51(1), 266-278.

[ 11] Tsang, R. H. L., & Ang, P. (2015). Cold temperature stress and predation effects on corals: their possible roles in structuring a nonreefal coral community. // Coral Reefs, 34 // (1), 97-108.

[ 12] Morton, B., & Blackmore, G. (2009). Seasonal variations in the density of and corallivory by Drupella rugosa and Cronia margariticola (Caenogastropoda: Muricidae) from the coastal waters of Hong Kong:‘plagues’ or ‘aggregations’?. // Journal of the Marine Biological Association of the United Kingdom, 89 // (1), 147-159.

[ 13] Hoeksema, B. W., Scott, C., & True, J. D. (2013). Dietary shift in corallivorous Drupella snails following a major bleaching event at Koh Tao, Gulf of Thailand. // Coral Reefs, 32 // (2), 423-428.

[ 14] Baird, A. (1999). A large aggregation of Drupella rugosa following the mass bleaching of corals on the Great Barrier Reef. // Reef Research, 9 //, 6-7.

[15] Forde, M. J. (1992). Populations, behaviour and effects of Drupella cornus on the Ningaloo Reef, Western Australia. //Drupella cornus: A Synopsis. Department of Conservation and Land Management, Western Australia, 4550.//

[16] Cros, A., & McClanahan, T. (2003). Coral transplant damage under various management conditions in the Mombasa Marine National Park, Kenya. //Western Indian Ocean Journal of Marine Science, 2//(2), 127-136.

[17] Shafir, S., & Rinkevich, B. (2010). Integrated long-term mid-water coral nurseries: a management instrument evolving into a floating ecosystem. //University of Mauritius Research Journal, 16//, 365-386.

[18] Lam, K., Shin, P. K., & Hodgson, P. (2007). Severe bioerosion caused by an outbreak of corallivorous Drupella and Diadema at Hoi Ha Wan marine park, Hong Kong. 2//Coral Reefs, 26//(4), 893-893.

[19] The Gap Year Guidebook (2017). //Podvolunteers tells us of their 2016 successes//. Retrieved from http://www.gap-year.com/news/pod-volunteer-tells-us-of-their-2016-successes

[ 20] Taylor, J. D. (1978). Habitats and diet of predatory gastropods at Addu Atoll, Maldives. // Journal of experimental marine Biology and Ecology, 31 // (1), 83-103.

[ 21] Vermeij, G. J., & Carlson, S. J. (2000). The muricid gastropod subfamily Rapaninae: phylogeny and ecological history. // Paleobiology, 26 // (1), 19-46.

[ 22] Claremont, M., Reid, D. G., & Williams, S. T. (2011). Evolution of corallivory in the gastropod genus // Drupella //. // Coral Reefs, 30 // (4), 977-990.

[23] Turner, S. J. (1992). The egg capsules and early life history of the corallivorous gastropod Drupella cornus (Röding, 1798). //The Veliger, 35//(1), 16-25.

[24] Morton, B., Blackmore, G., & Kwok, C. T. (2002). Corallivory and prey choice by Drupella rugosa (Gastropoda: Muricidae) in Hong Kong. //Journal of Molluscan Studies, 68//(3), 217-223.

[ 25] Sam, S. Q., Toh, T. C., Kikuzawa, Y. P., Ng, C. S. L., Taira, D., Afiq-Rosli, L., ... & Chou, L. M. (2017). Egg capsules and veligers of the corallivorous muricid gastropod Drupella rugosa (Born, 1778). // Invertebrate Reproduction & Development //, 1-8.

[26] Richmond, M. D. (1997). //A guide to the seashores of Eastern Africa and the Western Indian Ocean islands//. Sida/Department for Research Cooperation, SAREC.

[27] Döring, M. (2015). //Drupella rugosa//. Retrieved from https://www.gbif.org/species/113490381

[28] Tan, R. (2016). //Drills//. Retrieved from http://www.wildsingapore.com/wildfacts/mollusca/gastropoda/muricidae/muricidae.htm

[ 29] Born, I. (1778) // Index rerum naturalium Musei Caesarei Vindobonensis. Verzeichniss der Natürlichen Seltenheiten des K.K. Naturalien Kabinets zu Wien. Erster Theil, Schalthiere. Pars 1, Testacea //. Retrieved from https://www.biodiversitylibrary.org/bibliography/11581#/summary

[30] Global Biodiversity Information Facility (n.d.). //Drupella rugosa//. Retrieved from https://www.gbif.org/species/4363679

[31] Global Biodiversity Information Facility (n.d.). //Purpura alveolata//. Retrieved from https://www.gbif.org/occurrence/1056799360

[32] Johnson, M. S., & Cumming, R. L. (1995). Genetic distinctness of three widespread and morphologically variable species of Drupella (Gastropoda, Muricidae). //Coral Reefs, 14//(2), 71-78.

[33] Cheng, K. (2016) S'pore temperatures rising at double global average. Retrieved from http://www.todayonline.com/singapore/singapore-growing-warmer-twice-global-average