Caitlin Grant11/29/15

Independent Study

Literature Review on the Red Tree Coral, Primnoa pacifica

The deep-sea is home to a diverse community of unique organisms that hold many elusive answers to our questions about the evolution of the wide expanse of marine biodiversity present in a habitat that proves difficult to explore and study. Described as an environment with limited light, nutrient availability and unique topography, inhabiting species have had to adapt and specialize to reproduce and survive in these ecosystems(Watling et al., 2011).

Among the marine taxa present, octocorals have been highlighted in recent years as a species of interest, (Waller et al., 2014; Roberts et al., 2006) in part to its particular vulnerability to fishing disturbances, and more prevalent as of late, the impact of warming temperatures and changes in seawater chemistry may have on these corals (Roberts et al., 2006). Much of the wealth of knowledge already explored in octocorals is scattered, with gaps in many areas of octocoral reproduction, ecology and distribution.

In the 1800s, cold-water corals were discovered and found to be incredibly abundant, found in all ocean basins around the world at considerable depths (Watling et al., 2011). There are two major subclasses of cold-water corals: Hexacorallia, the hard corals, and Octocorallia, the soft corals. This review focuses on the subclass Octocorallia, which represents the most diverse group of corals, with 75% of the 3000 species known found in waters deeper than 50 m (Cairns, 2007a).

Octocorals are characterized by the subdivision of polyps by eight mesenteries consisting of tentacles containing lateral pinnules and tissues embedded with hardened sclerites (Watling et al., 2011). Within this subclass, 4 orders divide into Helioporacea, Alcyonacea, Gorgonacea, and Pennatulacea.

In the interest of this review, I have focused on species contained within the order Alyconacea. Order Alyconacea is further broken down into 6 suborders, one of which is the suborder Calcaxonia that embodies 5 families, 98 genera, all mostly distributed in deep waters, comprised of species with a solid axial skeleton, containing large amounts of non-scleritic calcareous material (Watling et al., 2011). Out of the 3 largest families within the suborder: Primnoidae, Chrysogorgiidae, and Isididae, Primnoidae has been identified as particularly abundant and diverse in deep waters, and are present in shallow water habitats as well (McFadden et al., 2006). Cairns & Bayer (2009) found cladistic evidence supporting the origination of Primnoidae in the Antarctic, where they are most abundant but found also in the North Pacific, North Atlantic and subantarctic South Pacific regions (Waller et al., 2014).

Called the “quintessential deep-water octocoral family” (Cairns & Bayer, 2009), Primnoidae is most common at bathyal-slope depths, with a vertical distribution of 8-5850 m (Watling et al., 2011). There are 233 valid species within the Primnoidae family,

making it the 4th largest octocorallian family, recognizable by the armor of scale-like sclerites covering their polyps (Watling et al., 2011).

Primnoidae’s ability to form large, branching thickets provide a suitable habitat for other invertebrate species, including polychaete worms, copepods, amphipods, and brittle stars (Coleman & Bernard, 1991). One such invertebrate, the polynoid worm Gorgoniapolynoe caeciliae has been observed to settle on colonies of the primnoid, Candidella imbricata. When the worm becomes 25 segments long, it creates “arbor-like” tunnels along the basal polyp sclerites, inducing changes in the corals morphology to support its growth (Ecklebarger et al., 2005). Due to these commensals utilizing these octocorals, any damage inflicted on these corals from fishing gear would also be causing habitat destruction to the invertebrates living within them.

In regards to food habits of deep-water and shallow-water corals, there are differences and crossovers in their preferences. Shallow-water gorgonians consume items such as phytoplankton, picoplankton, autotrophic nanoplankton, invertebrate eggs and detrital particulate organic matter (POM) (Orejas et al., 2003) and is likely that along with diatoms and dinoflagellates, deep-water species such as Primnoisis antarctica and the primnoid, Primnoella feed on these materials as well (Sherwood et al., 2008).

The red tree coral, Primnoa pacifica, has become a focal species in reproductive studies, due in part to its important role as a habitat forming octocoral and its distribution along shelf and upper slope areas, making it particularly vulnerable to fishing gear (Waller et al., 2014). In an effort to understand the extent of P. pacifica’s ability to recover from damage, it would be useful to conduct further studies on reproductive strategies, biogeographic patterns, and population connectivity (Watling et al., 2011). Primnoa pacfica is a long-lived, slow growing octocoral, and these disturbances have been seen to cause detrimental effects to their reproductive fitness, via planulae expulsion and resource allocation, reducing fecundity and possibly wiping out populations that would take years to return (Waller et al., 2014).

Preserving colonies of P. pacifica in the Gulf of Alaska, where a shallow-water population was recently discovered, is of particular interest to fishery managers due to the keystone refuge habitats P. pacifica provides for 12 species of rockfish (Sebastes sp.) (Waller et al., 2014). This shallow-water occurrence of normally deep-water P. pacifica is explained by Waller et al. (2014) as deep-water environments are being mimicked in shallow-water, high altitude fjords, a phenomenon termed “deep-water emergence.” Other coral species have been seen to adapt to different environments as well. Species of shallow-water Stylasteridae corals have been found to originate in the deep-sea. Although not well studied, Lindner et al. (2008) hypothesizes that in contrast to the stable deep-sea abyss, there are opportunities for the evolution and diversification of these corals to migrate into shallow, highly dynamic upper bathyal environments. Key deep-water characteristics provide evidence that supports deep-water corals in shallow-water fjord areas by both supporting nutrient-rich upwelling, low temperatures like bathyal depths, strong currents and low light levels (Waller et al., 2014).

Both the deep-water populations in the North Pacific and the shallow-water Tracy Arm habitats reside on shelf and upper slope areas, where limited energetic inputs and potential masked temporal and seasonal signals restrict energy available to octocorals to invest in reproduction (Watling et al., 2011). This restriction also affects external cues

necessary for gametogenetic development and spawning synchrony in populations of octocorals (Gage & Tyler, 1991; Young, 2003).

Most octocorals are gonochoristic, and both deep-sea corals and their shallow-water counterparts share common strategies of sexual reproduction (Watling et al., 2011). In P. pacifica, sexual reproduction occurs within the autozoids, as well as asexual reproduction via extratentacular budding along the central axis (Waller et al., 2014). There are two types of sexual reproduction that occur in octocorals: broadcast spawing, where fertilization and development occur in the water column, and brooding; where fertilization occurs within the maternal colony (Watling et al., 2011). Given the limitations in deep-sea octocorals’ energy stores for reproduction, internal fertilization and brooding would be predicted to be favored, however, deep-sea species of sea pens have been found to be exclusively broadcast spawners (Ecklebarger et al., 1998). Kahng et al. (2011) reported that internal brooding is a mode conserved among Primnoidae octocorals, but Waller et al. (2014) discredited this and confirmed that P. pacifica exhibits broadcast spawning instead. Alternately, soft corals in the Order Alyconacea, sometimes within the same genus, will exhibit both forms of sexual reproduction, showing a greater degree of reproductive flexibility (McFadden et al., 2001).

In deep-sea corals, several stages of developing oocytes or spermatocysts are commonly present in a single polyp, supporting a highly asynchronous method during gametogenesis (Rice et al., 1992). This feature was also observed by Waller et al. (2014) in P. pacifica, as well as a pattern among shallow-water species, suggesting a possible common phylogenetic feature of continuous gametogenesis in octocorals (Watling et al., 2011). Primnoa pacifica also shows seasonality trends in reproductive processes, Waller et al., (2015) collected samples from Eastern Pacific P. pacifica showing all four stages of spermatocytes present at one time.

Waller et al., (2014) found that the fecundity of vitellogenic oocytes seemed to be on more than a yearly cycle, as well as sperm maturation appearing to take just over a year to complete. These octocorals may extend the process of gametogenesis and oogenesis in an effort to synthesize larger, yolkier eggs (Orejas et al., 2007; Waller et al., 2014). This is also possibly to compensate for limited temporal cues, such as photoperiod, temperature and productivity peaks that effect synchronizing spawning activity (Watling et al., 2011). Waller et al. (2014) also noted that during spermatogenesis, corals may only be able to produce germ cells on yearly cycles and may only be able to mature oocytes sporadically when suitable conditions are present. The availability of food and lipid synthesis both affect these reproductive cycles (Waller et al. 2014) and need to be taken into consideration on top of possible anthropogenic activities harmful to the species. Due to the pulses at which plankton become available to these corals, this food availability cannot be relied on to fuel year round reproduction, based on the vertically distributed habitat (Waller et al. 2014).

The deep-water and the shallow-water populations of the red tree coral, P. pacifica, show many similarities in terms of reproduction, ecology, and environments. Given that this species is slow growing, with recruitment events seen to be on a decadal scale (Waller et al., 2014), this species is particularly vulnerable to fishing pressures, especially the larger, more reproductive colonies. Primnoa pacifica is also known as an ecosystem engineer that will change the local environment, providing a microhabitat for

colonization of associated species (Waller et al., 2014). Further research should be conducted in an effort to continue finding relationships between the two different habitats where P. pacifica flourishes to better understand how human interactions may negatively affect this species.

Works Cited

Cairns, S. D. (2007a). Studies on western Atlantic Octocorallia (Coelenterata: Anthozoa). Part 8: New records of Primnoidae from the New England and Corner Rise sea- mounts. Proceedings of the Biological Society of Washington. 120, 243-263.

Coleman, C. O. and Barnard, J. L. (1991). Amatiguakius forsberghi, a new genus and species from Alaska (marine Amphipoda: Epimeriidae). Proceedings of the Biological Society of Washington. 104, 279-287.

Eckelbarger, K. J., Tyler, P. A. and Langton, R. W. (1998). Gonadal morphology and gametogenesis in the sea pen Pennatula aculeata (Anthozoa: Pennatulacea) from the Gulf of Maine. Marine Biology. 132, 677-690.

Eckelbarger, K. J., Watling, L. and Fournier, H. (2005). Reproductive biology of the deep-sea polychaete Gorgoniapolynoe caeciliae (Polynoidae), a commensal species associated with octocorals. Journal of the Marine Biological Association of the United Kingdom. 85, 1425-1433.

Gage, J. D. and Tyler, P. A. (1991). Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor, Cambridge University Press, Cambridge.

McFadden, C. S., France, S. C., Sanchez, J. A. and Alderslade, P. (2006). A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Molecular Phylogenetics and Evolution. 41, 513-527.

Orejas, C., Gili, J. M. and Arntz, W. E. (2003). Role of small-plankton communities in the diet of two Antarctic octocorals (Primnoisis antarctica and Primnoella sp.). Marine Ecology Progress Series. 250, 105-116.

Rice, A. L., Tyler, P. A. and Paterson, G. J. L. (1992). The pennatulid Kophobelemnon stelliferum (Cnidaria: Octocorallia) in the Porcupine Seabight (North-east Atlantic Ocean). Journal Marine Biological Association of United Kingdom. 72, 417-434.

Roberts, J. M., Wheeler, A. J., Freiwald, A. (2006). Reefs of the Deep: The biology and geography of cold-water coral ecosystems. Science. 312, 543-547.

Sherwood, O., Jamieson, R. E., Edinger, E. N. and Wareham, V. E. (2008). Stable C and N isotopic composition of cold-water corals from the Newfoundland and Labrador continental slope: Examination of trophic, depth and spatial effects. Deep-Sea Research. I 55, 1392-1402.

Waller, R. G., Stone, R. P., Johnstone, J., Mondragon, J. (2014) Sexual Reproduction and Seasonality of the Alaskan Red Tree Coral, Primnoa pacifica. PLoS ONE 9,1-14.

Waller, R. G., Feehan, K. A. (2015). Notes on reproduction of eight species of Eastern Pacific cold-water octocorals. Jour. of Mar. Biol. Assoc. of Uni. King. 95, 691-696.

Watling et al. (2011). Chapt Two: Biology of deep-water octocorals. Advances in Marine Biology. 60, 41-122.

Young, C. M. (2003). Reproduction, development and life-history traits. In Ecosystems of the Deep Oceans (P. A. Tyler, ed), pp. 381-426. Ecosystems of the world. Vol. 28. Elsevier, Amsterdam.