Identification of the nutritional resources of larval sea lamprey in two Great Lakes tributaries using stable isotopes

Abstract

The sea lamprey (Petromyzon marinus) is an important invasive parasitic species in the Laurentian Great Lakes, but the nutritional subsidies supporting the protracted filter feeding ammocoete stage are not well established. We used stable isotope ratios (δ¹³C and δ¹⁵N) to determine the major sources of autochthonous (aquatically produced) and allochthonous (terrestrially produced) organic matter (OM) to the nutrition of ammocoetes collected in 2010 from the Pigeon and Jordan Rivers in Michigan (USA). Ammocoete δ¹³C was positively correlated with animal length and C:N ratio, but δ¹⁵N was not correlated with either, suggesting that ammocoetes are primary consumers. We used a Bayesian model (MixSIR) to estimate the contributions of potential nutritional sources to ammocoetes. Estimates suggest that aquatic sediments were most important to ammocoete nutrition (median contributions ranged from 49–51%). Aquatic plants, including macrophytes and algae, were also important to ammocoete nutrition with a median contribution of 29%. Terrestrial plants were generally of lesser but still significant importance to ammocoetes, with a median contribution of 19–39%. Our findings generally agree with those of previous studies that have found that inputs of detrital and recently living OM from aquatic primary producers both provide an important source of nutrition for ammocoetes. The present study provides more quantitative estimates of the different forms of OM supporting ammocoete nutrition and biomass.

Introduction

Invasion of the Laurentian Great Lakes by the parasitic sea lamprey (Petromyzon marinus) has fundamentally altered the structure and function of this ecosystem (Christie et al., 2003). The majority of the sea lamprey life cycle is spent as a sediment-dwelling, filter-feeding larva (i.e., the ammocoete stage) (Manion and Smith, 1978, Potter, 1980). The methods historically employed to visually identify ingested items within the ammocoete gut have suggested that algae are an important source of ammocoete nutrition (Moore and Mallatt, 1980, Mundahl et al., 2005, Sutton and Bowen, 1994). However, visually based methods cannot identify either the composition of the large detrital component in guts or the nutritional resources assimilated, rather than simply ingested, by the animals (Grey et al., 2002, Michener and Kaufman, 2007).

Early studies of sea lamprey ammocoete food and nutrition using gut content analysis (GCA) described the presence of “microscopic organisms” in the diet but downplayed the role of the far more dominant detrital organic matter (OM) (Applegate, 1961). Other GCA studies identified microalgae, in particular diatoms, as being critical to the diet of sea lamprey ammocoetes (Manion, 1967, Moore and Beamish, 1973, Moore and Mallatt, 1980). However, Manion (1967) noted that the ingestion of diatoms was correlated with diatom abundance in the water column, and suggested diatoms are only seasonally important. Later work by Sutton and Bowen (1994) and Mundahl et al. (2005) examined the entirety of the gut, and these authors argued that while algae could be important to ammocoete nutrition, ammocoete gut content was generally dominated by undifferentiated amorphous detrital material. For example, Sutton and Bowen (1994) found that > 92% of the ammocoete gut consisted of detrital OM.

Stable isotopic analysis (SIA) represents a potentially more robust and quantitative approach than GCA for assessing the nutritional source(s) of OM to organisms (Solomon et al., 2011). Naturally occurring isotopes of C and N in OM may be used to both qualitatively and quantitatively assess OM sources supporting an organism's nutrition, provided the isotopes of these elements can be measured in both the potential food sources and the consumer (Michener and Lajtha, 2007, Peterson and Fry, 1987, Post, 2002). Simultaneous use of multiple isotopes can better resolve the nutritional sources supporting consumers (Caraco et al., 2010, Cole et al., 2011, Peterson and Fry, 1987). Some naturally occurring stable isotopes can also be used to help establish at which trophic level organisms are feeding. For example, δ¹⁵N fractionates at ~ 3‰ for each trophic level providing wide differentiation, while δ¹³C fractionates only ~ 0–1‰ per trophic level (Peterson and Fry, 1987).

The objectives of the present study were to identify and quantify the dominant nutritional resources contributing to sea lamprey ammocoete biomass in two Laurentian Great Lakes tributaries. We predicted that sea lamprey ammocoete isotopic values would reflect nutritional contributions not only from aquatic OM, but also to a significant extent from allochthonous terrestrially derived detrital OM, owing to the dominance of terrestrially derived OM in streams and rivers (Cole et al., 2007, Cole et al., 2011).