Facing the Green Threat: A Water Flea's Defenses against a Carnivorous Plant

Abstract

Every ecosystem shows multiple levels of species interactions, which are often difficult to isolate and to classify regarding their specific nature. For most of the observed interactions, it comes down to either competition or consumption. The modes of consumption are various and defined by the nature of the consumed organism, e.g., carnivory, herbivory, as well as the extent of the consumption, e.g., grazing, parasitism. While the majority of consumers are animals, carnivorous plants can also pose a threat to arthropods. Water fleas of the family Daphniidae are keystone species in many lentic ecosystems. As most abundant filter feeders, they link the primary production to higher trophic levels. As a response to the high predatory pressures, water fleas have evolved various inducible defenses against animal predators. Here we show the first example, to our knowledge, in Ceriodaphnia dubia of such inducible defenses of an animal against a coexisting plant predator, i.e., the carnivorous bladderwort (Utricularia x neglecta Lehm, Lentibulariaceae). When the bladderwort is present, C. dubia shows changes in morphology, life history and behavior. While the morphological and behavioral adaptations improve C. dubia's survival rate in the presence of this predator, the life-history parameters likely reflect trade-offs for the defense.

Keywords: Daphnia; carnivorous plant; inducible defenses.

Figure 1

Morphological changes in C. dubia as a response to the presence of U. x neglecta. (A) Body length measurements over a duration of 6 days for four different treatments including two control treatments and two Utricularia-exposed treatments. (B) Normalized body widths (body width/body length). Utricularia-exposed animals show significantly smaller body length and normalized body width than the control treatments. * p < 0.05; ** p < 0.01; *** p < 0.001.

Figure 2

3D analysis of morphological alterations between control and Utricularia-exposed C. dubia. Control (A) and Utricularia-exposed C. dubia (B) of same age, scale bar = 1 mm. All subsequent analyses are projected on the average Utricularia-exposed animal. (C) Overall deformation; strong shifts are colored in shades of red, while small or no changes are indicated by shades of blue. (D) Confidence ellipsoid plot, revealing no overlapping confidence ellipsoids. (E,F) Here, shades of red indicate a shift in positive direction on that axis (dorsal/anterior/distal), shades of blue indicate a shift in negative direction on the respective axis (ventral/posterior/proximal). Shifts along the anterior–posterior (E) and dorso–ventral axis (F) show that the animals are smaller in the Utricularia-exposed morph. The deformation in the lateral dimension (G) gives regions of reduced and increased body width. Most of the found shifts are proven significant with respective Wilcoxon tests and FDR-based q-values (H,I,K). These figures give regions with p-values of respective Wilcoxon tests lower than 0.01 colored yellow, regions that also showed q-values lower than 0.001 are colored red. For the respective analysis, all samples of both treatments were taken into account (n_induced = 8, n_control = 13).

Figure 3

Changes in life history (in terms of clutch size alterations) of C. dubia in the presence of U. x neglecta. C. dubia revealed smaller clutch sizes (p ≤ 0.01) in the presence of U. x neglecta compared to the control treatments from day 4 onwards, stagnating at about one egg per female. * p < 0.05; ** p < 0.01; *** p < 0.001.

Figure 4

Changes in behavior in C. dubia observed as averaged distribution pattern with respect to the presence of either U. x neglecta or E. canadensis. (A) The box plots indicate the number of animals per column in the canvas drawn on the tank front pane. Increasing numbers on the x axis are equal to an increase in distance to the respective plant used in that treatment (1 equals to the same column as the plant, 6 is the opposite tank side). (B) The box plots indicate the number of animals per row. (C) The additional vector graph inlet is indicating the average positioning of the animals in respect to the plant by depicting a vector that represents the ‘calculated center of mass’ for every treatment as an offset from the tap water control treatment.

Figure 5

Behavioral changes in C. dubia as response to the presence of U. x neglecta: average duration (A) and velocity (B) of the two observed swimming modes in the ‘swimming modes’ experiments. (C) Survival rate of 20 five-day-old C. dubia (either control or Utricularia-exposed) over 24 h in the presence of 30 U. x neglecta traps. * p < 0.05; ** p < 0.01; *** p < 0.001.