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Notes on reproduction in the deep-sea cup coral Balanophyllia malouinensis (Squires 1961) from the Southern Ocean

May 2021
Polar Biology 44(5):1-10

Authors:

University of Gothenburg

Deep-sea scleractinian cup corals are prominent members of Southern Ocean megabenthic communities, though little is known about their life history. This study used paraffin histology and scanning electron microscopy to characterize the reproduction of the scleractinian coral Balanophyllia malouinensis (Squires, 1961) from Burdwood Bank in the Drake Passage. Samples were taken in April and May via otter trawls, Blake trawls, and dredges on three separate cruises: one on the RV Lawrence M. Gould in 2006, and two on the RV Nathaniel B. Palmer in 2008 and 2011. B. malouinensis is gonochoric with rare hermaphroditism. All four spermatocyst stages were seen simultaneously in males; similarly, most females contained oocytes at varying stages of development, though seasonality or periodicity could not be determined without a wider range of sample dates. Average fecundity was 241 ± 184 oocytes/individual (n = 38) and not correlated to cup size. Maturing larvae were found in the mesenteries and coelenteron of females, indicating B. malouinensis broods its larvae. This study was the first to characterize the reproduction of a deep-sea Balanophyllia species and adds to a small but growing body of work seeking to understand the unique benthic communities of Burdwood Bank.

Sampling Sites for Balanophyllia Samples and Example Specimens. a B. malouinensis samples were collected using trawls and dredges on Burdwood Bank on three separate cruises in May 2006 on the RV Lawrence M. Gould, and April 2008 and May 2011 on the RV Nathaniel B. Palmer. Data projected in EPSG 22194, overlaid with EPSG 4326 (WGS ’84) grid. B. malouinensis specimens, both alone (b) and attached (white arrow) to a larger Flabellum curvatum (c). Photo courtesy of Dann Blackwood, taken on cruise NBP08-03. Figure made in QGIS

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Histological Images of B. malouinensis Reproduction. Sections were stained with either H&E (a) or Masson’s trichrome (b, c). a Male section showing a range of spermatocyst stages (I-IV). Stage I spermatocysts were densely packed with spherical spermatids. Stage II spermatocysts stained a deep purple and had a “furry” look as gametes began to organize. Stage III spermatocysts had a highly distinctive open center. Stage IV spermatocysts were less dense, and flagella development created a “swirling” texture. b Several small pre-vitellogenic oocytes in female mesentery. c Large vitellogenic oocyte within a female. Images at 20X objective. Figure made in GIMP

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Early signs of development in B. malouinensis larvae. a Light histology section of individual larvae stained in H&E, labeled with internal septa (s). Image at 10X objective. b An SEM Micrograph displays external development of septa (s) and early oral disk (od). Figure made in GIMP

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Spermatocyst stages across male samples. Spermatocysts were classified from stage I to stage IV, in increasing maturity. a Percent frequency (%) of each stage per individual. Asterisks (*) represent hermaphrodites. b. Percent frequency (%) of each stage between months. Each point represents an individual; hermaphrodites were removed. Boxplots summarize the data per month and stage. Figure made in R

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Fecundity of April and May Individuals. Fecundity was estimated by counting oocytes in three mesenteries for each female individual. Thick bars represent the mean, and error bars represent the 95% confidence interval, with individual 69 (ID 69) excluded. The x-axis represents the categorical variable “month;” points were randomly jittered in the x-direction to allow easier visualization, but location on x-axis does not reflect differences in collection date between within each month. Figure made in R

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Polar Biology (2021) 44:977–986

https://doi.org/10.1007/s00300-021-02854-z

ORIGINAL PAPER

Notes onreproduction inthedeep‑sea cup coral Balanophyllia

malouinensis (Squires 1961) fromtheSouthern Ocean

AugustusPendleton1 · EliseHartill1· RhianWaller1

Received: 31 July 2020 / Revised: 6 February 2021 / Accepted: 25 March 2021 / Published online: 5 April 2021

Abstract

Deep-sea scleractinian cup corals are prominent members of Southern Ocean megabenthic communities, though little is

known about their life history. This study used paraﬃn histology and scanning electron microscopy to characterize the repro-

duction of the scleractinian coral Balanophyllia malouinensis (Squires, 1961) from Burdwood Bank in the Drake Passage.

Samples were taken in April and May via otter trawls, Blake trawls, and dredges on three separate cruises: one on the RV

Lawrence M. Gould in 2006, and two on the RV Nathaniel B. Palmer in 2008 and 2011. B. malouinensis is gonochoric with

rare hermaphroditism. All four spermatocyst stages were seen simultaneously in males; similarly, most females contained

oocytes at varying stages of development, though seasonality or periodicity could not be determined without a wider range

of sample dates. Average fecundity was 241 ± 184 oocytes/individual (n = 38) and not correlated to cup size. Maturing

larvae were found in the mesenteries and coelenteron of females, indicating B. malouinensis broods its larvae. This study

was the ﬁrst to characterize the reproduction of a deep-sea Balanophyllia species and adds to a small but growing body of

work seeking to understand the unique benthic communities of Burdwood Bank.

Keywords Coral· Deep sea· Reproduction· Southern Ocean· Scleractinian· Cold-water corals

Introduction

Most shallow-water zooxanthellate corals are hermaphro-

ditic, a reproductive pattern that may be enabled by abundant

food sources in sunlit waters (Harrison 2011). In contrast,

the deep sea is cold, dark, and dependent on food-fall from

the surface; however, a startling diversity of reproductive

strategies is observed for corals in this environment (e.g.,

Roberts etal. 2009). Of the deep-sea coral species for which

published results are available, only three are hermaphro-

ditic, all within the genus Caryophyllia and displaying

quasi-continuous gamete production and lecithotrophic lar-

vae (Waller etal. 2005). Other deep-sea scleractinians char-

acterized are gonochoric (Waller etal. 2008; Roberts etal.

2009; Mercier etal. 2011; Waller and Tyler 2011; Pires etal.

2014). These deep-sea species exhibit both seasonal, non-

seasonal, and periodic modes of gamete production. In the

absence of light, and with relatively stable temperature and

pH, it is hypothesized that changes in surface productivity

and subsequent marine snow ﬂuxes help regulate seasonal

reproduction in the deep sea (Tyler 1988). As reproduction

is characterized in more deep-sea coral species, the potential

drivers for the observed reproductive diversity will become

better understood.

Burdwood Bank is an undersea plateau oﬀ the Argen-

tinian shelf, to the north of the Drake Passage. This bank

has diverse benthic communities including many deep-sea

corals (Schejter and Bremec 2019). Located approximately

200 km south of the Falkland Islands in the Southern Ocean,

the plateau of Burdwood Bank is at most 200 m deep but

slopes steeply to nearly 3000 m deep on the Southern side

(Zunino and Ichazo 1979). The Drake Passage is dominated

by the eastward ﬂow of the Antarctic Circumpolar Current

and has strong vertical mixing (Arhan etal. 2002). As the

Antarctic Circumpolar Current contacts Burdwood Bank,

it rises up the slope, bringing nutrients from deeper waters

(Arhan etal. 2002). It is considered a sub-Antarctic area of

ecological importance with a diverse and vulnerable benthic

community rich in coral fauna (Schejter etal. 2016).

In 2013, Argentina created the Namuncurá Marine

Protected Area (NMPA) that encompasses approximately

* Augustus Pendleton

guspendleton@gmail.com

1 Darling Marine Center, University ofMaine, Walpole, ME,

USA

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

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This revision is the result of a study of the genotype species, mostly of type or topotype specimens, of nearly every described scleractinian genus. The classification proposed rests primarily on the structure of the septa, but other skeletal structures as well as the soft parts are utilized and considered. The order Scleractinia is divided into five suborders: Astrocoeniida, Fungiida, Faviida, Caryophylliida, and Dendrophylliida. The first is quite distinct from the others and includes corals with septa composed of relatively few trabeculae. The other four include corals in which the septa consist of a relatively large number of trabeculae. The Fungiida is marked by the fundamentally fenestrate arrangement of the trabeculae, whereas the arrangement is laminar in the Faviida, Caryophylliida, and Dendrophylliida. In the Faviida the septal margins are dentate; in the Caryophylliida they are smooth; and in the Dendrophylliida some septa may become secondarily lacerate or dentate. The subdivision of the suborders into lesser categories is based upon the modification of septal structure and other skeletal elements, mode of colony - formation, form of the corallum, and phylogeny of the groups. The systematic classification is prefaced by an historical résumé of previous investigations of the Scleractinia and a brief discussion of the anatomy and morphology of the polyps and skeletal structures. The several different modes of sexual and asexual reproduction and increase are carefully analyzed because of their relation to growth form and from this is developed a discussion of morphogenesis of the corallum. Considerable attention is paid to the ecology of recent corals—much is known concerning the reef-building forms, but certain aspects of the ecology of the ahermatypic or non-reef-builders are here extensively considered for the first time. The distribution of fossil and recent scleractinian faunas is broadly analyzed and some suggestions concerning the evolution of the order are made. A classified list of over a thousand titles dealing with all aspects of the Scleractinia and fifty-one plates illustrating nearly three-fourths of the approximately 500 genera recognized conclude the work.

Notes on reproduction in the deep-sea cup coral Balanophyllia malouinensis (Squires 1961) from the Southern Ocean

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