Effect of diet on the coupling of ingestion and egg production in the ubiquitous copepod, Acartia tonsa

Highlights

• Copepod ingestion and egg production rates are linearly related for most diets.

• Copepod egg production efficiency is strongly dependent on diet.

• The diatom diet shows the highest egg production efficiency.

Abstract

The ability of consumers to convert ingested carbon into growth is critical for secondary production and trophic transfer. We conducted laboratory experiments to investigate the effect of different prey and concentration on the ingestion rate (IR), egg production rate (EPR) and egg production efficiency (EPE) of the ubiquitous copepod, Acartia tonsa. Experiments were run at several prey concentrations, ranging from 11 to 1132 μgC L^–1, of the diatom Thalassiosira weissflogii, the autotrophic dinoflagellate Prorocentrum minimum, the heterotrophic dinoflagellate Oxyrrhis sp., the flagellate Dunaliella tertiolecta, and the bacterivorous scuticociliate Uronema sp. IR increased curvilinearly with concentration for all diets. EPR also increased curvilinearly with increasing food concentration similar to IR, with the exception of the flagellate diet, for which EPR decreased linearly with food concentration. EPR ranked as T. weissflogii > P. minimum > Oxyrrhis sp. = Uronema sp. > D. tertiolecta. IR and EPR were linearly related, except for flagellate diet. The slope of the carbon-based relationship between IR and EPR, the egg production efficiency (EPE), was highest for the diatom (77.5%) and lowest for the scuticociliate (4.2%). Egg production was not correlated to ingestion of the flagellate offered to A. tonsa. We conclude that of the five prey species, the diatom T. weissflogii is the best prey to promote A. tonsa reproduction, to optimize trophic transfer efficiency, and to increase mass cultivation of this species.

Introduction

Copepods, the most abundant metazoans in the oceans (Humes, 1994) and the dominant component of the mesozooplankton, are integral components of food webs and modulate the linkage between primary producers to upper trophic levels, thereby affecting fish recruitment (Runge, 1998). Through their processes of ingestion, growth, defecation and excretion, copepods play an important role in global biogeochemical cycles (Noji, 1991, Buitenhuis et al., 2006).

While ingestion constrains all elements of the bioenergetics budget, the coupling of ingestion and growth partly determines trophic transfer efficiency. A wide variety of autotrophic and heterotrophic protists in marine pelagic systems constitutes the food source for copepods (Kleppel, 1993). Both food quantity and quality affect copepod ingestion and fecundity. Food quality is defined by size (Nival and Nival, 1976, Durbin et al., 1983, Paffenhofer, 1984, Berggreen and Hansen, 1988), morphology (Donaghay and Small, 1979, Gifford et al., 1981), toxicity (e.g. Huntley et al., 1986, Ianora and Poulet, 1993, Ban et al., 1997, Colin and Dam, 2002, Colin and Dam, 2007, Teegarden et al., 2008, Ianora and Miralto, 2010), elemental and biochemical compositions (e.g. Ambler, 1986, Kiørboe, 1989, Jónasdóttir, 1994, Cowie and Hedges, 1996, Guisande et al., 2000, Jones et al., 2002, Broglio et al., 2003, Arendt et al., 2005, Thor et al., 2007, Nobili et al., 2013), and taxonomic composition (Kleppel et al., 1991, Wichard et al., 2007). Food elemental stoichiometry (C:N:P) relative to the needs of the grazers and availability of specific compounds such as fatty acids and sterols are also considered important determinants of ingestion and fecundity (Anderson et al., 2005, Vargas et al., 2006, Evjemo et al., 2008, Siuda and Dam, 2010, Chen et al., 2012, Nobili et al., 2013).

Food quality affects copepod growth. For example, declines in development and egg production are linked to diets deficient in elemental nutrient or some essential fatty acids in both autotrophic and heterotrophic diets (e.g. Kiørboe, 1989, Hessen, 1992, Jónasdóttir et al., 1995, Klein Breteler et al., 2005, Thor et al., 2007). Moreover, trophic upgrading or modification of food limited in essential lipids by heterotrophic protists has been documented (Ederington et al., 1995, Klein Breteler et al., 1999), and species-specific differences have been observed (Tang and Taal, 2005, Veloza et al., 2006).

The response of copepods to food in the form of egg production rate has commonly been used as a measure of nutritional adequacy. Yet, egg production is not always correlated with phytoplankton concentration and ingestion (White and Roman, 1992). The gross- growth efficiency is the percentage of ingested food that is allocated to growth. The median copepod gross-growth efficiency is ~ 20–30% (Straile, 1997), but with wide uncertainty (range: <5 to >60%), which is perhaps not unexpected from a meta-analysis of > 100 disparate studies that considered different predators and prey, prey concentration, and food quality.

The copepod Acartia tonsa is a ubiquitous cosmopolitan estuarine species that is often used in studies of copepod biology, and for mass cultivation for aquaculture. Hence, there is considerable interest in studying patterns of production in this species and understanding the mechanisms responsible for these patterns. A previous paper of ours examined the coupling between ingestion and defecation as a function of diet (several planktonic groups, motile and nonmotile prey) in Acartia tonsa (Besiktepe and Dam, 2002). That study observed linear relationships between ingestion and defecation, but strong differences among diets in absorption efficiencies. These, in turn, could lead to strong differences in coupling between growth and ingestion. In the present study we characterize the coupling of egg production and ingestion as a function of diet, which has implications for understanding and predicting trophic transfer efficiency.