Research Article: Ocean acidification influences plant-animal interactions: The effect of Cocconeis scutellum parva on the sex reversal of Hippolyte inermis

Date Published: June 26, 2019

Publisher: Public Library of Science

Author(s): Mirko Mutalipassi, Valerio Mazzella, Valerio Zupo, Gustavo M. Martins.


Ocean acidification (O.A.) influences the ecology of oceans and it may impact plant-animal interactions at various levels. Seagrass meadows located at acidified vents in the Bay of Naples (Italy) are considered an open window to forecast the effects of global-changes on aquatic communities. Epiphytic diatoms of the genus Cocconeis are abundant in seagrass meadows, including acidified environments, where they play key ecological roles. A still-unknown apoptogenic compound produced by Cocconeis triggers the suicide of the androgenic gland of Hippolyte inermis Leach 1816, a protandric hermaphroditic shrimp distributed in P. oceanica meadows located both at normal pH and in acidified vents. Feeding on Cocconeis sp. was proven important for the stability of the shrimp’s natural populations. Since O.A. affects the physiology of diatoms, we investigated if, in future scenarios of O.A., Cocconeis scutellum parva will still produce an effect on shrimp’s physiology. Cell densities of Cocconeis scutellum parva cultivated in custom-designed photobioreactors at two pH conditions (pH 7.7 and 8.2) were compared. In addition, we determined the effects of the ingestion of diatoms on the process of sex reversal of H. inermis and we calculated the % female on the total of mature individuals-1 (F/mat). We observed significant differences in cell densities of C. scutellum parva at the two pH conditions. In fact, the highest cell densities (148,808 ±13,935 cells. mm-2) was obtained at day 13 (pH 7.7) and it is higher than the highest cell densities (38,066 (±4,166) cells. mm-2, day 13) produced at pH 8.2. Diatoms cultured at acidified conditions changed their metabolism. In fact, diatoms grown in acidified conditions produced in H. inermis a proportion of females (F/mat 36.3 ±5.9%) significantly lower than diatoms produced at normal pH (68.5 ±2.8), and it was not significantly different from that elicited by negative controls (31.7 ±5.6%).

Partial Text

Hippolyte inermis Leach is a shrimp mainly inhabiting meadows of Posidonia oceanica [1] and in other seagrasses [2]. Hippolyte inermis is a key component of their food webs, as a link between primary producers, fishes and other carnivores [3]. The shrimp naturally undergoes a process of protandric sex reversal [4,5].

This study aimed at investigating how O.A. can affect the cell density of Cocconeis scutellum parva benthic diatoms simulating the present status (pH 8.2) and a hypothetical future condition (pH 7.7). Since the shrimp H. inermis is the only known “biological sensor” that is able to track the presence of the active apoptogenic compound produced by the diatom, the effects of Cocconeis spp. cultivated at the two pH scenarios on shrimps’ post-larvae diet was examined to test its potential effect on plant-animal interactions. To compare the effects of C. scutellum parva, C. scutellum posidoniae, a strictly related variety that has been proved to be able to produce apoptogenic metabolite [26], was also tested as positive control.

Our results demonstrated that Cocconeis scutellum parva cultured at acidified conditions (pH 7.7) produced four times more cells than the same diatoms cultured at normal conditions (pH 8.2). The pCO2 recorded at pH 7.7 is quite higher (about 4 times) then the one recorded at pH 8.2 and, similarly, the cell densities recorded at pH 7.7 are significantly higher (about 4 times) than the ones recorded at pH 8.2. In fact, the time trends of cell densities are significantly correlated to the pCO2. Our results on the growth of C. scutellum parva in photobioreactors are in accordance with studies performed at Castello Aragonese meadows, where species populating the vent include a suite of organisms resilient to naturally high concentrations of pCO2 and the massive presence of Cocconeis sp. may indicate that these species may have a competitive advantage under low pH conditions, in the field. The effect of CO2 on the growth of diatoms is quite complex and, probably, depends on the particular physiology of each species. It has been shown that species can use different carbon sources, with some utilizing CO2 as main carbon source, whereas others mostly drawing carbon from HCO3- [35]. Elevated CO2 concentration did not cause significant differences in growth in diatoms such as Asterionella glacialis, Thalassiosira punctigera, Coscinodiscus wailesii, Phaeodactylum tricornutum [36–38]. In the case of Chaetoceros gracilis, the maximum number of cells was obtained at a carbon dioxide concentration of 385 μatm and a lower cell number was obtained at lower (control and 280 μatm) and higher levels of carbon dioxide (1,050 μatm) [35]. In other species, such as Thalassiosira weissflogii, algal density decreased with the decreasing pH [39] probably because, when the acidity is lower than a certain concentration, it will impair algal physiological functioning [40]. In contrast, previous studies [41] demonstrated an advantage of larger planktonic diatom species, more than 40 μm in diameter, over smaller-sized ones with an enhanced growth rate under elevated pCO2 due to a combination of increased diffusion rates, a lowering of metabolic costs and a lower susceptibility to photo-inactivation of PSII.