Linking nutrient inputs, phytoplankton composition, zooplankton dynamics and the recruitment of pink snapper, Chrysophrys auratus, in a temperate bay

Abstract

Survival of larval fish is often linked to production of preferred prey such as copepods, both inter- and intra-annually. In turn, copepod production depends not only the quantity of food, but also on the nutritional quality, edibility and/or toxicity of their micro-algal food. Hence, larval fish survival can become de-coupled from levels of nutrient input depending on the resulting composition of the plankton. Here we use a plankton dynamics model to study nutrient input, phytoplankton composition and copepod, Paracalanus, production in relation to interannual variation in recruitment of snapper, Chrysophrys auratus, in Port Phillip Bay, Australia. The model was able to simulate the ratio of diatoms to flagellates in the plume of the main river entering Port Phillip Bay. Interannual variability in the copepod, Paracalanus, abundance during the C. auratus spawning period over 5 years was accurately predicted. The seasonal peak in Paracalanus production depended on the timing and magnitude (match-mismatch) of nutrient inputs and how these were reflected in temporal change in the diatom:flagellate ratio. In turn, the model-predicted Paracalanus abundance was strongly related to inter-annaul variability in abundance of snapper, C. auratus, larvae over 7 years. Years of highest larval C. auratus abundance coincided with a matching of the spawning period with the peak in Paracalanus abundance. High freshwater flows and nutrient inputs led to an early seasonal dominance of diatoms, and consequently reduced abundances of copepods over the C. auratus spawning period with correspondingly low abundances of larvae. Conversely years of very low rainfall and nutrient input also led to low phytoplankton and copepod concentrations and larval C. auratus abundances. Highest abundances of larval C. auratus occurred in years of low to intermediate rainfall and nutrient inputs, particularly when pulses of nutrients occurred in the spring period, the latter supporting the match-mismatch hypothesis.

Introduction

Recruitment variability is a key driver of the population dynamics of many marine fish stocks (Thorson et al., 2014) and is often found to be independent of reproductive potential (Morgan et al., 2011). One of the foundation hypotheses to explain recruitment variability in marine fish stocks was put forward by Hjort (1914), and held that there was a critical period at the point of first feeding by larvae where the presence of suitable amounts and types of food would determine year-class strength. In the intervening years, other hypotheses relating to recruitment variability such as the match-mismatch hypothesis (Cushing, 1969, Cushing, 1990) and the growth-mortality hypothesis (Houde, 1987, Anderson, 1988) have extended Hjort's original hypothesis to a broader focus encompassing the entire pelagic larval phase characterised by high mortality (Houde, 2008), and potentially extending into the early juvenile phase (Campana, 1996).

The match-mismatch hypothesis is based on the observation that spawning times of marine fish species are often relatively fixed, while the timing of production of planktonic prey can be much more variable (Cushing, 1969, Cushing, 1990). The hypothesis was originally applied to the spring plankton bloom in temperate marine systems that occurs with the onset of stratification, but may be equally applicable to other systems where the timing of plankton production is variable in relation to the fish spawning period (Cushing, 1990). The growth-mortality hypothesis links poor nutrition and consequent slow growth of larvae with increased size-dependent mortality, most likely caused by size- or growth-selective predation (Houde, 2008).

Larval survival may be influenced not only by the amount but also by the type of prey. Fish larvae are commonly found to be selective feeders, and, in particular, the life stages of calanoid copepods are often found to be preferred prey (Robert et al., 2014), particularly at higher latitudes (Llopiz, 2013). Interannual variation in copepod production has been found to strongly influence recruitment success of some species (Beaugrand et al., 2003, Castonguay et al., 2008).

Like larval fish, production of mesozooplankton such as copepods depends not only on per capita prey availability but also on the nutritional quality, edibility and/or toxicity of their micro-algal food (Poulet et al., 1994, Lee et al., 1999, Nejstgaard et al., 2001, Paffenhöfer et al., 2005). The composition and abundance of phytoplankton communities can vary depending on a range of factors, including; availability of micro- and macro-nutrients, light, temperature, turbulent mixing and grazers (Margalef, 1978, Reynolds, 2006, Litchman and Klausmeier, 2008). Nutrient availability is a key factor that can influence both community composition and the nutritional quality of phytoplankton cells (Klein Breteler et al., 2005, Litchman et al., 2007, Litchman and Klausmeier, 2008). Diatoms are a dominant group within the marine phytoplankton that are typically favoured under high nutrient conditions (Reynolds, 2006, Litchman et al., 2007). Numerous studies have, however, shown that some diatoms contain compounds, collectively termed oxylipins, which can inhibit copepod growth and reproduction (Paffenhöfer, 2002, Ianora et al., 2003, Paffenhöfer et al., 2005, Lauritano et al., 2012). In contrast to diatoms, flagellates typically prosper in conditions of lower macro-nutrient (i.e. nitrate, phosphate, silicate) concentrations because smaller species of phytoplankton are better adapted to growth under low nutrient conditions and they don't require silicate (Eppley et al., 1969, Aksnes and Egge, 1991, Egge and Aksnes, 1992, Diekmann et al., 2009). Overall, diatoms or flagellates will be favoured under different concentrations of silicate and nitrate, and therefore nutrient concentrations are a major determinant of the diatom:flagellate ratio. It is clear that considering only total phytoplankton abundance (e.g., measures of Chl a) without consideration of the composition of the phytoplankton will often be insufficient to predict production at higher trophic levels.

The pink snapper, Chrysophrys auratus (Sparidae), supports a highly important commercial and recreational fishery in sub-tropical and temperate Australia (Kailola et al., 1993). The Western Victorian Stock of snapper straddles the south-east Australian states of Victoria and South Australia, with Port Phillip Bay in central Victoria the main spawning area for this stock (Hamer et al., 2011). The Western Victorian Stock is characterised by high recruitment variability (Hamer and Jenkins, 2004) that is likely to be a major driver of population dynamics.

Studies on snapper in Port Phillip Bay have indicated that recruitment variability is likely to be driven by environmental factors that affect the larval stage, particularly food availability and to a less extent water temperature (Murphy et al., 2012, Murphy et al., 2013, Murphy et al., 2014). Snapper larvae in Port Phillip Bay preferentially select calanoid copepod nauplii in the early larval stage, and calanoid copepodites and cladocerans in the later stage (Murphy et al., 2012). Nauplii and copepodites of the calanoid copepod Paracalanus were found to be key preferred prey (Murphy et al., 2012). The dietary niche breadth, in terms of the dominance in the diet of these preferred prey, was found to be correlated with inter-annual variation in larval abundance, suggesting a link between production of preferred prey and larval survival (Murphy et al., 2012). Years of higher abundance were also characterised by faster growth in the early stage (Murphy et al., 2013). In turn, larval growth was found to be related to production of copepod nauplii and water temperature (Murphy et al., 2013). Finally, using daily increment analysis of larvae and juveniles, Murphy et al. (2014) found daily larval mortality was a function of per capita prey availability for three cohorts.

Although these studies provide multiple lines of evidence that abundance of preferred prey is critical to the survival of snapper larvae in Port Phillip Bay, there is still not a clear understanding as to what extent inter-annual variation in larval survival is a result of overall differences in prey production amongst years, or rather the match-mismatch of spawning period and prey production within years (Cushing, 1990). Some evidence for the latter was found by Murphy et al. (2014) where within-year, as well as between-year variation in larval mortality was found to be related to per capita prey availability.

In this paper, we use a plankton dynamics model to explore the relationship between nutrient inputs, plankton production and snapper larval abundance across 7 years spanning a range of nutrient inputs related to drought and post-drought conditions. In particular, we evaluate the relative roles of aggregate inter-annual variation in plankton production versus the match or mismatch of intra-annual variation in production with the snapper spawning period. We hypothesise that de-coupling of nutrient inputs and C. auratus recruitment can be explained by changes in phytoplankton composition in response to nutrient inputs and subsequent impacts on zooplankton, particularly copepod availability for larval fish.