Growth rate consequences of coloniality in a harmful phytoplankter

Abstract

Background: Allometric studies have shown that individual growth rate is inversely related to body size across a broad spectrum of organisms that vary greatly in size. Fewer studies have documented such patterns within species. No data exist directly documenting the influence of colony size on growth rate for microscopic, colonial organisms.

Methodology/principal findings: To determine if similar negative relationships between growth rate and size hold for colonial organisms, we developed a technique for measuring the growth of individual colonies of a bloom-forming, toxic cyanobacterium, Microcystis aeruginosa using microscopy and digital image analysis. For five out of six genotypes of M. aeruginosa isolated from lakes in Michigan and Alabama, we found significant negative relationships between colony size and growth rate. We found large intraspecific variation in both the slope of these relationships and in the growth rate of colonies at a standard size. In addition, growth rate estimates for individual colonies were generally consistent with population growth rates measured using standard batch culture.

Conclusions/significance: Given that colony size varies widely within populations, our results imply that natural populations of colonial phytoplankton exist as a mosaic of individuals with widely varying ecological attributes (since size strongly affects growth rate, grazing mortality, and migration speed). Quantifying the influence of colony size on growth rate will permit development of more accurate, predictive models of ecological interactions (e.g., competition, herbivory) and their role in the proliferation of harmful algal blooms, in addition to increasing our understanding about why these interactions vary in strength within and across environments.

Figure 1. Microcystis aeruginosa colony size measurements.

The surface area and width of individual colonies was measured using microscopy and digital image analysis. Example measurements for individual colonies of three M. aeruginosa genotypes ((A) HudsonBD02, (B) MagicianA02, and (C) SwanBO02) measured on days 1 and 5. Stippled white line was traced with a mouse for estimation of surface area. Solid white line represents our approximation of colony depth (see text for explanation). For HudsonBD02 (A), the perimeter of the void in the center of the colony was also traced and its estimated surface area was subtracted from the total surface area. All photos taken at 63× magnification.

Figure 2. Patterns between Microcystis aeruginosa colony growth rate and size.

Relationship between growth rate (day⁻¹) and initial colony equivalent spherical diameter (ESD, mm) measured between days 1 and 8 for individuals of three M. aeruginosa genotypes (HudsonBD02, MagicianA02, and SwanBO02) grown in chambered microscope slides.

Figure 3. Test of colony resource exhaustion.

(A) Relationship between growth rate (day⁻¹) and initial colony equivalent spherical diameter (ESD, mm) between days 1 and 7 for individual colonies of four M. aeruginosa genotypes (ALB3R708, Erie31F1206, HudsonBD02, and SwanBS02). (B) Comparison of colony growth rates for small colonies of four M. aeruginosa genotypes grown in chambered slides in isolation (dark bars) or in association with a large colony of the same genotype (white bars). Error bars = 1 standard error. Inset numbers are sample sizes.

Figure 4. Population and colony growth rate comparison.

Growth rates for five Microcystis aeruginosa genotypes (GilkeyL02, HudsonBD02, MagicianA02, GullNO3E1-206, SwanBO02) grown in batch culture (flasks, dark bars) versus individual colonies grown in chambered slides (white bars). Error bars = 1 standard error. Inset numbers are sample sizes.