Hidden defensive morphology in rotifers: benefits, costs, and fitness consequences

Abstract

To cope with predation, many prey species have developed inducible defenses in terms of morphology, behavior, and life history. Rotifers were the first model organisms used to evaluate the ecology and evolution of inducible defenses in aquatic ecosystems. Since the middle of last century, only visible morphological defenses, such as spine development, have been found and only in a few rotifer species. Given the development of ultrastructural defenses is taxonomically widespread in aquatic ecosystems, we hypothesize that rotifer prey, particularly small-sized species, can develop such inducible defenses. We evaluated morphological response of two common Brachionus herbivores (B. calyciflorus and B. angularis) to predatory rotifer Asplanchna brightwellii. Results confirmed existence of predator-induced ultrastructural defenses, which are expressed as increased lorica thickness and enhanced lorica hardness. Such inducible defenses are more evident and effective in the smaller sized B. angularis, leading to higher fitness of B. angularis in predator-prey interactions. As anticipated, development of defenses has inevitable fitness costs manifested as decreased reproduction or reduced sex investment. Our results not only extend understanding of inducible ultrastructural defense to other planktonic taxa that were previously observed only in cladocerans, but also verify effective mechanical protection of such hidden defensive morphology.

Figure 1

Biometric characters of Brachionus calyciflorus (left) and Brachionus angularis (right) measured in the present study. (A) body length; (B) body width; (C) length of posterolateral spine. White filled circles indicate the tested areas on each rotifer under atomic force microscopic observations. Scale bar = 100 µm.

Figure 2

Prey ingestion rate (the percentage of the number ingested to number of successful captures) and prey ingestion time (time from the successful capture of prey by jaw to ingestion of captured from mastax to stomach) of Asplanchna brightwellii fed Brachionus calyciflorus (B.c.) and Brachionus angularis (B.a.) cultured in the medium with (K⁺) and without (K⁻) Asplanchna kairomones. To minimize the potential influences of body size and presence of attached eggs on feeding preference of A. brightwellii, we conducted the experiments with newborn B.c. (<1 h old) and non-ovigerous adult B.a. (>24 h old). Body length of B.c. in K⁻ = 137.0 ± 1.2 µm (n = 30); Body length of B.c. in K⁺ = 150.8 ± 1.4 µm (n = 30); Body length of B.a. in K⁻ = 124.6 ± 1.2 µm (n = 30); Body length of B.a. in K⁺ = 122.3 ± 1.4 µm (n = 30). Prey ingestion rate = 100 × (number of ingestion/number of successful capture); Prey ingestion time = time from successful capture of prey by jaw to ingestion of captured from mastax to stomach. Data of prey ingestion rate are mean ± S.E. based on 15 replicated observations within 10 min. Data of prey ingestion time are mean ± S.E. based on 15 replicated recordings.

Figure 3

Boxplots of production and mixis ratio of offspring in Brachionus calyciflorus and Brachionus angularis cultured in the medium with (K⁺) and without (K⁻) Asplanchna kairomones. The solid horizontal line is the median and the triangle is the mean. The deviation bars represent the 5^th and 95^th percentiles, whereas the dots show the 1^th and 99^th percentiles. Data shown are based on 64 replicated Brachionus mothers.

Figure 4

Survival of Brachionus calyciflorus (B.c.) and Brachionus angularis (B.a.) cultured together with Asplanchna brightwellii. At each prey combination, B.c. and B.a. cultured in the medium with (K⁺) and without (K⁻) Asplanchna kairomones are provided with proportion of 50%: 50% (25 individuals from each species). We conducted the experiments with newborn B.c. and non-ovigerous adult B.a. (see the legend in Fig. 3 for the detailed explanation). Data are mean ± S.E. based on 12 replicated observations.

Figure 5

Population dynamics of Brachionus angularis (B.a.) and Brachionus calyciflorus (B.c.) fed with Chlorella pyrenoidosa at a concentration of 1 mg C L⁻¹. Left: B.a. and B.c. were co-cultured without predator. Right: B.a. and B.c. were co-cultured under predation risk (Asplanchna brightwellii = 100 ind. L⁻¹). Data shown are mean ± standard error values based on six replicates.