Past energy allocation overwhelms current energy stresses in determining energy allocation trade-offs

Abstract

Regeneration of lost appendages is a gradual process in many species, spreading energetic costs of regeneration through time. Energy allocated to the regeneration of lost appendages cannot be used for other purposes and, therefore, commonly elicits energetic trade-offs in biological processes. We used limb loss in the Asian shore crab Hemigrapsus sanguineus to compare the strength of energetic trade-offs resulting from historic limb losses that have been partially regenerated versus current injuries that have not yet been repaired. Consistent with previous studies, we show that limb loss and regeneration results in trade-offs that reduce reproduction, energy storage, and growth. As may be expected, we show that trade-offs in these metrics from historic limb losses far outweigh trade-offs from current limb losses, and correlate directly with the degree of historic limb loss that has been regenerated. As regenerating limbs get closer to their normal size, these historical injuries get harder to detect, despite the continued allocation of additional resources to limb development. Our results demonstrate the importance of and a method for identifying historic appendage losses and of quantifying the amount of regeneration that has already occurred, as opposed to assessing only current injury, to accurately assess the strength of energetic trade-offs in animals recovering from nonlethal injury.

Keywords: Asian shore crabs; Hemigrapsus sanguineus; energetic trade‐offs; limb regeneration; nonlethal injury; regeneration.

FIGURE 1

Methods for determining which limbs were regenerating in Hemigrapsus sanguineus. Data shown are for the right claw. There is no significance in the choice of this specific limb, as similar relationships were observed for all limbs. (a) Residual limb masses from the nonlinear regression of limb mass on carapace width. Limbs that fall below the red vertical line are assumed to be regenerating. (b) Allometric relationship between limb mass and carapace width. Limbs shown in red are assumed to be regenerating (i.e., these are the limbs that fell below the red line in part a).

FIGURE 2

Cardiac stomach mass of Hemigrapsus sanguineus (after accounting for body size and day of year) was not significantly influenced by the number of limbs missing (a), showed a unimodal relationship with the number of limb buds started (b), and was only weakly influenced by the mass of historically missing limbs that had already formed (c). Residuals used for visual presentation purposes only. Positive and negative residuals reflect, respectively, stomach masses that are larger or smaller than expected for a given carapace width at that time of year. The dashed horizontal line in each graph highlights the zero point of no change. In each boxplot, the heavy line shows the median, the box encompasses the 1st to 3rd quartile, the whiskers extend to 1.5× this interquartile range, and the circles show outliers that fall outside this range.

FIGURE 3

Residual ovary mass of Hemigrapsus sanguineus (after accounting for body size and day of year) was not significantly influenced by the number of limbs missing (a), decreased with the number of limb buds that have started (b), and decreased with the cumulative mass of the historically missing limbs that had already formed (c). Residuals used for visual presentation purposes only. Positive and negative residuals reflect, respectively, ovary masses that are larger or smaller than expected for a given carapace width at that time of year. Boxplots and dashed line are as described in the caption to Figure 2.

FIGURE 4

Residual hepatopancreas mass of Hemigrapsus sanguineus (after accounting for body size and day of year) decreased with the number of missing limbs (a), and with the number of limb buds that have started (b), and with the cumulative mass of the historically missing limbs that had already formed (c). Residuals used for visual presentation purposes only. Positive and negative residuals reflect, respectively, hepatopancreas masses that are larger or smaller than expected for a given carapace width at that time of year. Boxplots and dashed line are as described in the caption to Figure 2.

FIGURE 5

Residual expected body mass (after accounting for body size and day of year) was not significantly influenced by the number of limbs missing (a), but increased with the number of limb buds that have started (b), and decreased with the cumulative mass of the historically missing limbs that had already formed (c). Residuals used for visual presentation purposes only. Positive and negative residuals reflect, respectively, body masses that are larger or smaller than expected for a given carapace width at that time of year. Boxplots and dashed line are as described in the caption to Figure 2.