Immune Response in Crayfish Is Species-Specific and Exhibits Changes along Invasion Range of a Successful Invader

Abstract

Immunity is an important component of invasion success since it enables invaders' adaptation to conditions of the novel environment as they expand their range. Immune response of invaders may vary along the invasion range due to encountered parasites/microbial communities, conditions of the local environment, and ecological processes that arise during the range expansion. Here, we analyzed changes in the immune response along the invasion range of one of the most successful aquatic invaders, the signal crayfish, in the recently invaded Korana River, Croatia. We used several standard immune parameters (encapsulation response, hemocyte count, phenoloxidaze activity, and total prophenoloxidaze) to: i) compare immune response of the signal crayfish along its invasion range, and between species (comparison with co-occurring native narrow-clawed crayfish), and ii) analyze effects of specific predictors (water temperature, crayfish abundance, and body condition) on crayfish immune response changes. Immune response displayed species-specificity, differed significantly along the signal crayfish invasion range, and was mostly affected by water temperature and population abundance. Specific immune parameters showed density-dependent variation corresponding to increased investment in them during range expansion. Obtained results offer baseline insights for elucidating the role of immunocompetence in the invasion success of an invertebrate freshwater invader.

Keywords: body condition; crayfish abundance; hepatosomatic index; immune response; water temperature.

Figure 1

Partial least squares regression (PLS-R) score plots of signal crayfish immune parameters, based on y components (u1 and u2). Plots represent the relationship between response variables (immune parameters) and predictors (water temperature, relative crayfish abundance (CPUE), Fulton’s condition factor (FCF), and hepatosomatic index (HSI)) according to sites along invasion range (a), upstream and downstream river segments (b), and invasion core and front sites (c). Significant effect (p < 0.01) in ‘response-predictor’ relation (performed by using the generalized linear model on PLS-R scores) is indicated with **. DC = downstream invasion core, DF = downstream invasion front, UC = upstream invasion core, UF = upstream invasion front.

Figure 2

(a) Radar of correlation, illustrating the relationship between response variables (signal crayfish immune parameters, represented with blue lines) and predictors (represented with red lines). (b) Standardized coefficients of signal crayfish immune response. The closer to the absolute value of 1 the coefficient is, the stronger the effect of that predictor on the response variable (controlling for other variables in the equation). (c) Variable importance for the projection (VIP) for explanatory variables of first two components (t1 and t2). VIP > 1 indicate the explanatory variables that contribute the most to the PLS model. CPUE = catch per unit effort (relative crayfish abundance), FCF = Fulton’s condition factor, HSI = hepatosomatic index, PO = phenoloxidaze, proPO = prophenoloxidaze, THC = total hemocyte count.

Figure 3

Principal component analysis (PCA) biplot on immune parameters of the signal crayfish and narrow-clawed crayfish from their mixed populations. Variables are indicated by black arrows, where their length represents the influence of a specific variable in shaping a model. 95% confidence ellipses are estimated around clusters. PO = phenoloxidaze, proPO = prophenoloxidaze, THC = total hemocyte count.