Asexual diapause induced by food limitation in the rotifer Synchaeta pectinata

Ecology, June, 1998 by John J. Gilbert, Dorothee K. Schreiber

INTRODUCTION

Many organisms become inactive or undergo some type of dormancy to survive when the environment is unsuitable for growth and reproduction. For example, microorganisms may transform into or produce spores or cysts (Henis 1987), annual and perennial plants produce seeds with varying periods of dormancy (Meyer and Kitchen 1992), and metazoans may hibernate, estivate, cease development or reproduction, or produce a variety of dormant stages. In freshwater invertebrates, dormant stages include gemmules (sponges), statoblasts (bryozoans), and resting eggs (turbellarians, rotifers, and microcrustaceans) (see Pennak 1989). Induction of an inactive or dormant phase may be triggered by a factor associated with a deteriorating environment or by some environmental cue that predicts either an unfavorable environment some time in the future or an environment especially suitable for the development of a dormant stage. The present paper describes the initiation of a newly-discovered, short-term diapause stage in rotifers by food limitation. This diapause response should increase fitness in environments where food concentrations during the growing season intermittently decrease below those necessary for positive population growth.

Many monogonont rotifers have heterogonic life cycles (Gilbert 1980, 1983, 1992, 1993). During a growing season, reproduction is primarily by diploid female parthenogenesis, but there may be one or more periods when some proportion of the population reproduces sexually. Sexuality is initiated by an environmental stimulus that induces amictic (female-producing) females to produce mictic (male-producing) daughters. Such stimuli have been identified in only a few species: increasing population density in Brachionus, dietary tocopherol in Asplanchna, and long photoperiod in Notommata and Trichocerca. Mictic females lay haploid eggs, which develop parthenogenetically into males or which are fertilized by males and develop into encysted, energy-rich, diapausing embryos called resting eggs. These eggs can remain viable in sediments for many years and then hatch into amictic females. Resting eggs provide a long-term refuge from unfavorable conditions and permit clones to persist from one growing season to another.

The life cycle of the common planktonic rotifer Synchaeta pectinata is more complex and flexible than that known in other rotifers. Sexuality, and consequently the production of fertilized resting eggs, may occur. However, in addition, many clones of this species have a unique option for an asexually-produced diapause stage (Gilbert 1995, Gilbert and Schreiber 1995). Well-fed, amictic females produce typical, thin-shelled amictic eggs that are subitaneous and develop without arrest into females. However, when these females are subjected to a period of starvation, they are likely to produce amictic eggs that enter diapause in an early stage of development. Depending on the clone, these diapausing eggs have a shell of greater but varying thickness, contain one or several (2-8) nuclei, and hatch automatically after about 1 wk or several mo (Gilbert 1995; S. C. Fradkin, unpublished observations). Such diapausing eggs probably increase clonal fitness by providing a refuge from food limitation during periods of fluctuating food availability within a single growing season.

The diapausing amictic eggs of S. pectinata are unusual for several reasons. First, the brief (1-2 wk) diapause of the eggs of some clones is in marked contrast to the long-term diapause usually associated with fertilized resting eggs in rotifers, cladocerans, and copepods (Gilbert 1974, Moritz 1987, Marcus et al. 1994, Hairston et al. 1995). Second, the production of diapausing amictic eggs by S. pectinata appears to be one of very few cases in aquatic metazoans in which diapause is induced by food limitation or in which diapause is consequential (see Begon et al. 1996), directly triggered by an environmental factor that decreases fitness. In most examples of diapause in aquatic metazoans, the diapause is predictive, or induced by a cue, such as photoperiod, that is not directly inhibitory. In aquatic systems, diapause induced by nutrient or food limitation appears to be common only in microorganisms (Corliss and Esser 1974, Fryxell 1983, Fenchel 1987, Whitton 1987, Brock et al. 1994).

In the present study, we experimentally test several hypotheses regarding the nature of the food-limitation stimulus that induces diapausing amictic eggs in S. pectinata. More specifically, we consider the conditions that may lead to the induction of these eggs in natural systems and address the mechanism causing their induction. Previous studies showed only that well-fed, young adults soon began to produce diapausing eggs after being subjected to a 12- or 15-h period of starvation (Gilbert 1995, Gilbert and Schreiber 1995). Rotifers in natural systems, of course, would be unlikely to experience such an abrupt reduction in food availability. We hypothesize that rotifers continuously exposed to low food concentrations over an entire generation will produce diapausing eggs. We also hypothesize that young adults transferred from a high food concentration to a lower one for various periods of time will be increasingly likely to produce diapausing eggs as the concentration of the low-food pulse decreases and as the duration of the low-food pulse increases. Rotifers in natural ecosystems could experience these regimes if the food available to them gradually fluctuated over the course of a growing season or was patchily distributed, respectively. Finally, we test the hypothesis that decreased birth rate may be the direct trigger for the diapause response. We do this by exposing well-fed rotifers to a toxic cyanobacterium to reduce fecundity independently of food availability.