Using latent effects to determine the ecological importance of dissolved organic matter to marine invertebrates

Synopsis

The uptake and utilization of dissolved organic matter (DOM) by marine invertebrates is a field that has received significant attention over the past 100 years. Although it is well established that DOM is taken up by marine invertebrates, the extent to which it contributes to an animal's survival, growth, and reproduction (that is, the ecological benefits) remains largely unknown. Previous work seeking to demonstrate the putative ecological benefits of DOM uptake have examined them within a single life stage of an animal. Moreover, most of the benefits are demonstrated through indirect approaches by examining (1) mass balance, or (2) making comparisons of oxyenthalpic conversions of transport rates to metabolic rate as judged by oxygen consumption. We suggest that directly examining delayed metamorphosis or the latent effects associated with nutritional stress of larvae is a better model for investigating the ecological importance of DOM to marine invertebrates. We also provide direct evidence that availability of DOM enhances survival and growth of the bryozoan Bugula neritina. That DOM offsets latent effects in B. neritina suggests that the underlying mechanisms are at least in part energetic.

Introduction

All organisms ranging from the simplest bacterium to the most sophisticated multicellular animal need energy for maintenance, growth, and reproduction, and a wide variety of mechanisms supplying that energy have evolved. One such system that has developed among aquatic organisms involves the cellular transport and utilization of dissolved organic matter (DOM) directly from the surrounding medium. It is well known that heterotrophic bacteria and protozoans use this abundant source of carbon and nitrogen for growth and reproduction (for example, Crawford and others 1974; Williams and others 1976; Williams 2000). Although first hypothesized over 100 years ago for metazoans such as sponges and cnidarians (see Jorgensen 1976 for a historical review), early progress in DOM research suffered from difficulties associated with measuring minute fluxes of DOM relative to large ambient concentrations. The application of more sophisticated technologies such as radiotracer studies and HPLC led to a renewed interest in the field during the past several decades and, although we have a very good understanding of the types of compounds involved and the rates of transport, the actual contribution of DOM to the nutrition, growth, reproduction, and survival of marine invertebrates remains largely unknown. The paucity of data in this area is in part due to lack of a good model systems for testing the ecological effects of DOM. In the few cases where experiments have been performed, researchers have exclusively looked for effects within a single life stage of an animal (for example, Ferguson 1980).

Over the past few decades biologists studying marine invertebrates have begun to recognize and demonstrate that events occurring in one portion of a life cycle can have dramatic and long-lasting effects at another stage in the life cycle (see Pechenik and others 1998; Pechenik 2006; this volume for recent reviews). For example, delayed metamorphosis or short-term nutritional stress of larvae can affect postmetamorphic growth, survival, or reproduction in many marine invertebrates (for example, Woollacott and others 1989; Miller 1993; Wendt 1998; Phillips 2002; Wacker and von Elert 2002). Following Pechenik (2006) we use the term "latent effects" to refer to such phenomena. We suggest that examining latent effects in embryos or larvae are a novel and direct method of determining the ecological importance of DOM transport. We also suggest that this approach provides a suitable test for the hypothesis that certain latent effects are mediated in part through depletion of larval energy reserves (for example, Pechenik and Eyster 1989; Pechenik and others 1993; Wendt 1998; Thiyagarajan and others 2002; Marshall and others 2003; reviewed by Pechenik and others 1998; Pechenik 2006).

In this paper we will provide ( 1 ) a brief review of what is known about the importance of DOM for growth, reproduction, and survival of marine invertebrates, (2) an overview of latent effects that result from delayed metamorphosis or nutritional stress, (3) a discussion of previous ways of determining the importance of DOM to marine invertebrates, (4) the results from a model system that utilized a direct examination of latent effects to determine ecological importance of DOM, and (5) suggestions for other suitable means of investigating the longstanding and as yet unanswered question-does DOM matter for marine invertebrates?

Importance of DOM for growth, reproduction, and survival of marine invertebrates

The earliest reports of the use of DOM by invertebrates date back to the latter part of the 19th century. Formal investigation of utilization of DOM by marine invertebrates was first widely acknowledged by August Putter (1908) who measured oxygen consumption for a marine protozoan and determined that energy gained from clearing food particles from seawater was probably not sufficient to support the organism's basal metabolic rate. Indeed, he showed that the protozoan would have to remove all the food contained in 9.4 liters of seawater in 1 h to support its metabolism. This indirect evidence led Putter to invoke the use of DOM as a possible supplement to meet basic metabolic needs. His suggestion was further supported by additional calculations showing that the DOM necessary to support the organism's metabolic demand was contained in about 0.5 ml of seawater. Putter's conclusions, however, are necessarily based on accurate measurement of several variables as follows: (1) metabolic rate, (2) concentrations of DOM, (3) concentration of particulate food, and (4) clearance rates. Clearly, inaccuracies in any of these parameters could substantially change the strength of his conclusions. In fact, Krogh (1931) pointed out that Putter had greatly underestimated phytoplankton concentrations and greatly overestimated the abundance of DOM. Krogh went on to cite other investigators who called into question Putter's measurement of metabolic rates, specifically maintaining that his estimates were probably too high. In Krogh's (1931) critical and extensive review he generally concluded "that there is no convincing evidence that any animal takes up dissolved organic substances from natural water in any significant amount..." but he also stated in his conclusions that there is "strong evidence from experiments... that tadpoles, mussels, and probably many other animals can absorb organic substances from fairly concentrated solutions and at least for a considerable period thrive and grow without particulate food." In sum, Krogh's basic conclusions were that animals at artificially high concentrations have the ability to take up and even utilize DOM, but they do not have this capacity to any appreciable extent under natural conditions. That is, the uptake and utilization of DOM, according to Krogh, is not significant at ecologically realistic concentrations.