Physiological response of the hydromedusa Cladonema californicum Hyman (Anthomedusa: Cladonemidae) to starvation and renewed feeding

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1 Journal of Experimental Marine Biology and Ecology, 225 (1998) L Physiological response of the hydromedusa Cladonema californicum Hyman (Anthomedusa: Cladonemidae) to starvation and renewed feeding John Costello Biology Department, Providence College, Providence, RI , USA Received 13 November 1996; received in revised form 11 July 1997; accepted 25 July 1997 Abstract Field studies have identified food limitation as a factor influencing medusae in their natural environment. Whereas previous laboratory studies have focused on food limitation of large cruising medusae, this study examines the effect of starvation on a small ambush predator, the hydromedusa Cladonema californicum Hyman. C. californicum survived periods of starvation lasting up to 45 days without significant mortality; renewed feeding resulted in resumed growth and development. Small ( 1 mm) to medium ( 2 mm) diameter medusae were relatively insensitive to periods of up to one week without food. In fact, these medusae appeared to continue growing during this period. However, elemental analysis (CHN) measurements demonstrated two characteristics of C. californicum s starvation response. First, apparent growth (increases in diameter but not weight) resulted from organic (dry weight, carbon, nitrogen) dilution of body tissues. Second, true growth (increases in both diameter and weight) occurred only when minimum carbon levels were reached in medusan tissues. The minimum carbon concentrations allowing true growth depended upon medusan size Elsevier Science B.V. Keywords: Medusa; Starvation; Gelatinous; Predation; Invertebrate; Body size 1. Introduction Predators rarely enjoy a uniformly available food source. Instead, prey are more typically dispersed in clumped or patchy distribution patterns. This is particularly true of marine plankton (Haury et al., 1978; Hamner and Carleton, 1979). Periods of negative energy balance, or starvation, may alternate with periods of positive energy balance, or growth. A number of potential responses to food shortage occur among plankton. Some copepods reduce metabolic rates during diapause. This strategy allows survival through extended periods of low food availability but results in lowered assimilation efficiency / 98/ $ Elsevier Science B.V. All rights reserved. PII S (97)

2 14 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) and reduced ability to utilize temporarily variable food resources (Landry and Hassett, 1985). An alternative response to environments of fluctuating food availability is the storage of lipid rich energy reserves. Although this is common among planktonic crustaceans (Lee, 1974; Sargent, 1976), gelatinous marine invertebrates do not typically form lipid rich energy reserves (exceptions are noted in Larson and Harbison, 1989). Instead, their bodies are predominantly formed of proteinaceous tissues (Ikeda, 1972; Percy and Fife, 1981; Arai et al., 1989). For these organisms, starvation endurance and efficient collection of scarce prey are critically important for surviving periods of low food availability. Field studies indicate that starvation tolerance may be an important factor influencing populations of medusae. Zelickman et al. (1969) found little or no food in the guts of Barents Sea hydromedusae and suggested that alternative food sources such as inorganic nutrient uptake or phytophagous nutrition must occur for such hydromedusae. Larson (1986) found that medusan abundance in Saanich Inlet, British Columbia was closely related to prey densities, suggesting food limitation as the primary influence on medusan population dynamics. Olesen et al. (1994) implicated food limitation as an influential factor affecting populations of the scyphomedusae Aurelia aurita in the shallow ford, Kertinge Nor, Denmark. Thus, as has been suggested for crustacean zooplankton (Dagg, 1977; Lampert and Muck, 1985), the ability of gelatinous predators to endure variable food supplies probably acts as a strong selective force. Previous research has demonstrated a consistent pattern which has become a model for medusan response to food limitation. Hamner and Jenssen (1974) found that the scyphomedusan predator, A. aurita, endured periods of starvation by metabolizing body tissue and decreasing body mass through a process termed degrowth. While degrowth resulted in a progressive decrease in bell diameter as body tissues were catabolized, subsequent feeding resulted in regrowth and bell diameter increase. Arai (1986) described a similar pattern for the hydromedusa Aequorea victoria experiencing starvation and renewed feeding. Arai et al. (1989) subsequently found that, with the exception of a small decline in the glucose levels during the first 3 days of starvation, A. victoria utilized carbohydrate, protein and lipid body components at similar rates. Based on these previous studies, the medusan response to starvation entails an essentially non-selective catabolism of all body components and a concomitant decrease in size. Whereas in many animal groups, large size confers greater resistance to starvation (Threlkeld, 1976; Peters, 1983; Millar and Hickling, 1990), gelatinous predators have no biochemical advantage due to energy reserves associated with larger size. In fact, Larson (1986) argued that small size would be favored among gelatinous predators facing food limitation because weight specific respiration is relatively constant for all medusan sizes and smaller members of a population would be more likely to obtain their necessary maintenance ration than larger individuals during periods of low food availability. Size characteristics of field populations of the scyphomedusa A. aurita appear to support this view; they are characterized by low average bell diameter during periods of prey scarcity (Olesen et al., 1994). Costello (1992) has suggested that the degrowth response of A. aurita and A. victoria may be characteristic of medusae which are cruising foragers, but that ambush predators might show a different response to starvation. Ambush foraging medusae sit relatively

3 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) motionless with tentacles extended and wait for prey to encounter their tentacles. Although these medusae may swim to a new area (Mills, 1981) their feeding behavior involves limited active searching for prey. Of the variables Gerritsen and Strickler (1977) considered (relative population densities, speeds of predator and prey, encounter radii) in their model of planktonic foraging patterns, encounter radius had the greatest influence on the encounter probabilities between predator and prey. Therefore, increased encounter radius may confer an advantage to medusan predators which ambush their prey. In this case, limited size decreases might be expected to accompany degrowth during starvation by ambush medusan predators. Development of culture methods (Costello, 1988) and basic nutritional background information (Costello, 1991) for a medusan ambush predator, Cladonema californicum Hyman, has provided an opportunity to evaluate this issue. 2. Methods 2.1. Culture and growth of medusae Cladonema californicum medusae (Fig. 1) were collected from polyps maintained in continuous laboratory culture (Costello, 1988). Three cohorts were collected and grown at 188C. Each of the three cohorts budded asexually from the same colonies on different days and were grown to different bell diameters prior to experimentation. The sizes of the three different cohorts at the time of experimentation were: small (6 days old, 1.4 mm diameter), medium (13 days old, 2.0 mm diameter), and large (35 days old, 3.0 mm diameter). Numbers of individual medusae in each size cohort varied from approximately 900 (large medusae) to over 3000 (small medusae). Small medusae, Fig. 1. Figurative cross section a 2.5 mm diameter Cladonema californicum medusa. Medusan volume (insert) was calculated as the difference between the two spheres determined from the exterior and interior subumbrellar diameters, respectively.

4 16 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) especially when starved, had low biomass and respiration values and therefore required larger numbers of individuals per sample. Each size class of medusae was fed to satiation with 4 day old Artemia sp. nauplii until used for experimentation Sampling scheme The intent of the sampling scheme was to follow alterations in body mass (measured as dry weight [DW], carbon [C] and nitrogen [N]) and metabolism (measured as respiration) through the course of starvation and subsequent renewed feeding. The sampling regime involved holding a portion of each cohort without food for 28 days (Fig. 2) while, at week intervals, subgroups were refed. The time course of changes in bell diameter, DW, C, N and respiration were then measured for both starved and refed medusae. Sampling of the starved groups occurred at 3 4 day intervals. Sampling of the refed medusae occurred on the first, third and seventh days after renewed feeding. For each of these sample periods, sample animals were removed prior to feeding for that day. Previous work (Costello, 1988) demonstrated that digestion occurred within 8 h of feeding. Therefore, it is unlikely that residual prey in the guts of refed medusae influenced C, N or DW measurements. All size groups followed the same basic regime shown in Fig. 2 but, instead of Fig. 2. Basic sample regime for starvation and renewed feeding experiments with Cladonema californicum medusae. A large cohort of each size group (small, medium, large) was subjected to the basic regime. Symbols represent dates on which samples were collected for size (bell diameter) biomass (carbon, nitrogen, dry weight) and respiration. Empty circles represent samples taken during continuous starvation; filled symbols represent small groups of medusae which were removed from the larger starved cohort and fed to satiation daily. Renewed feeding trials occurred after the first, second and third weeks of the 28 day long starvation regime. Each renewed feeding trial lasted seven days, and sampling occurred on the first, third and seventh day of renewed feeding. See text for deviations from this regime.

5 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) terminating at 28 days as did the small and large groups, the medium group was maintained unfed for 45 days in order to examine the effect of longer starvation periods. No samples were taken from the medium group between day 28 and day 45. Some other minor variations occurred in the sampling regime. For example, during the second renewed feeding trial of the medium size group, sampling occurred on the second and third, rather than the first and third days of renewed feeding Body size and respiration measurements Bell diameter was measured with a Zeiss dissecting microscope equipped with an ocular micrometer calibrated to 0.02 mm. The bell diameters of a minimum of 25 medusae were measured for each sample period. Bell volume measurements assumed that the medusan bell could be approximated as a sphere (Fig. 1). However, the exterior bell volume actually consists of a relatively thin walled body enclosing an interior fluid-filled, subumbrellar cavity (Fig. 1). The volume of the subumbrellar cavity was subtracted from the exterior volume to determine the volume of medusan tissues. Both external and subumbrellar volumes were approximated as spheres; direct measurements indicate that the subumbrellar cavity diameter was approximately 89% (SD 3.4%, n 5 23) of the exterior bell diameter. Body mass was measured in terms of DW, C and N. Samples for DW determinations were rinsed in distilled water, dried at 608C in a pre-weighed aluminum boat, and weighed on a Cahn microbalance to mg. C and N content were determined for dried, weighed samples on a Perkin Elmer CHN analyzer. Three CHN samples were collected at each sample period. Respiration rates were measured using a modification of the Winkler method (Strickland and Parsons, 1972) for small volumes ( ml) as described by Costello (1991). Seven respiration measurements and 3 controls (no medusae added to seawater) were taken for each sample period Statistical analysis Differences between major class variables (size group, treatment, day) were tested for significance by ANOVA and ANCOVA. If differences between class variables were significant, the Tukey s honest significant difference test (HSD, adjusted for unequal N) was used for post-hoc multiple comparisons of sample means. For example, if ANOVA indicated that a significant difference in bell diameter existed within a particular size group between sample dates, the Tukey s HSD test was used to discriminate on which dates bell diameters differed significantly from each other for that size group. 3. Results 3.1. Effects of starvation on body size, composition and respiration The effects of starvation on bell diameter differed by size class (ANCOVA, p, 0.001, Fig. 3). There were no significant differences in bell diameter of large medusae between

6 18 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Fig. 3. Average bell diameter for small, medium and large size groups during starvation. Error bars represent 95% confidence intervals based on the standard error of the mean. Error bars exist for each data point; where no bars are evident, they are small enough to be covered by the graphic symbol. days 1 and 3. After that, bell diameter of the large group decreased consistently with day 28 significantly less than all previous dates. The small and medium groups did not shrink immediately after food became available. Instead, bell diameter increased significantly during the first three days of starvation (Tukey s HSD, p, 0.05 for both small and medium groups) before stabilizing in these groups. After stabilizing, bell diameter fluctuated non-significantly, and, in the medium group, tended to decrease. However, after 28 days of starvation, average bell diameter of the small and medium groups had still not declined below pre-starvation levels. Even after 45 days, the medium group had shrunk to only 2 0.6% of the pre-starvation bell diameter. This was not a significant size decrease relative to the pre-starvation bell diameter (Tukey s HSD, p 5 1.0). Shrinkage was greatest in the large group; however, even in this group, the average bell diameter reduction after 28 days of starvation was less than 11% (Table 1). Increased bell diameter of the small and medium groups during the initial days of the starvation period were not due to increased biomass. DW, C and N content of all size classes declined throughout the starvation period in similar proportions. Respiration rate per medusae showed similar decreases to those of major body constituents (Table 1, Fig. 4). The ratio of C:N declined during starvation but remained in the range of 3.5 to 4.7, indicating that proteins dominated the body composition of C. californicum. The C:N ratios of the small and medium groups were not significantly different during the

7 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Table 1 Percentage decrease of Cladonema californicum medusan biomass and metabolic rates during the course of starvation experiments Size group Diameter Dry Carbon Nitrogen Respiration Carbon weight density Small (1) Medium (1) Large (1) Denotes an increase. starvation period. However, the C:N ratios of the large medusae were significantly higher than the other two groups during starvation (Tukey s HSD, p,.001). In terms of C content, the three size groups responded to starvation similarly when normalized for both initial C content and body volume (Fig. 5). There were no significant differences in percentage decrease of body C between size groups during starvation (ANCOVA, p , Fig. 5) nor in C density (C content normalized for bell volume). Therefore, although patterns of bell diameter varied between groups, all sizes showed similar patterns of biomass changes. These losses were substantial during the 28 day period common to all size classes, ranging from 69 77% for DW, C and N (Table 1). Decreases in respiration were slightly greater, ranging from 75 83%. Although the medium sized medusae had greater losses at 45 than 28 days without food; the period of greatest decline was during the first two weeks of starvation (Fig. 5). In summary, biomass (described by DW, C and N) and metabolic rate declined similarly during the 28 day period of starvation for all three size classes of C. californicum. In contrast, bell diameter did not show similar dramatic declines and actually increased during the initial days of starvation for small and medium medusae. This resulted in a dilution of organic content of all size classes during starvation Effects of renewed feeding on body size and composition Renewed feeding did not result in immediate bell diameter increases for any size class of C. californicum. With the exception of the medium size class group starved for 1 wk, significant increases in bell diameter were recorded on only the seventh day of renewed feeding (Fig. 6). The medium group starved 1 wk increased in diameter more rapidly; a significant increase occurred after only 3 days of renewed feeding. Carbon content of medusae did not mirror bell diameter changes. Significant increases in C between sample dates were more frequent during renewed feeding and were evident after 1 day in several of the small and medium renewed feeding trials (Fig. 7). Although there was a clear trend of increasing C content in the large medusae during renewed feeding, variability within sample dates obscured the statistical significance of average increases between dates. The length of time required to return to pre-starvation C content levels increased with bell diameter between size classes; small medusae generally recovered most rapidly whereas large medusae required the longest time period for recovery (Fig. 7, Table 2).

8 20 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Fig. 4. Time course of biomass and respiration changes for the three size groups during starvation. Error bars represent 95% confidence intervals based on the standard error of the mean. Error bars exist for each data point; where no bars are evident, they are small enough to be covered by the graphic symbol. The coupling between bell diameter and body C content was a threshold dependent relationship. After a period of starvation, increased C content was coupled with increased bell diameter only when the average C per medusa exceeded the level characteristic of pre-starvation medusae (Fig. 8). In other words, significant bell diameter growth of medusae which had been starved occurred only when the medusae had fed enough to regain the C levels (as well as other body constituents such as DW and N) that characterized their period of high growth prior to starvation. Thus, for each

9 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Fig. 5. Time course of changes in body carbon during starvation for small, medium and large cohorts of starving Cladonema californicum. No error bars are associated with these data because the values are determined from the ratios of values which are themselves averages. Percentage decrease in carbon is the average carbon value on a sample date normalized by the initial value in the time series. Carbon density is the average carbon measurement on a sample date normalized by the average medusan volume on that sample date. size class, there appeared to be a threshold C content necessary for growth in bell diameter. Below that threshold, increased C content per medusa was uncoupled from significant increases in bell diameter (Fig. 8). 4. Discussion Cladonema californicum is clearly capable of enduring starvation for long periods, at least 28 days, and recovering when food becomes available. All size classes were

10 22 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Fig. 6. Effect of renewed feeding on bell diameter of starved Cladonema californicum medusae. Pre-starvation level refers to the average bell diameter at the outset of the starvation experiment. Asterisks denote values that are significantly greater (Tukey s HSD, p,0.05) than those of preceding sample days. capable of recovery after losing the bulk of their C content (. 74%). Other indicators of biomass such as DW and N, showed similar but slightly lower decreases during starvation. Starvation tolerance of this magnitude is unusual in the animal kingdom. Kleiber (1961) described a generalized rule termed Chossat s rule: animals die when total weight loss reaches half the initial body mass. C. californicum reached less than 50% of initial body weight with no adverse long term effects (Table 1). A. aurita can probably survive even greater weight loss (Hamner and Jenssen, 1974). Excluding diapausing crustaceans, starvation tolerance of C. californicum is long compared to most zooplankton. By combining weight specific respiration rates with Chossat s rule, Threlkeld (1976) derived the equation

11 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Fig. 7. Effect of renewed feeding on carbon content of individual Cladonema californicum medusae during starvation. Pre-starvation level refers to the average medusan carbon content at the outset of the starvation experiment. Asterisks denote values that are significantly greater (Tukey s HSD, p,0.05) than those of preceding sample days t W to predict survivorship of starving crustacean zooplankton at 208C where t represents survival time (days) and W represents initial DW (mg). This formula assumes protein metabolism during starvation. Application of this formula to C. californicum predicts survival of only 8, 11 and 14 days for small, medium and large medusae, respectively. Clearly, these medusan predators do not fit this scheme. Although starvation tolerance of this magnitude is uncommon among animal phyla, it is well documented among other medusae. Hamner and Jenssen (1974) starved the

12 24 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Table 2 Recovery times (in days) required for starved Cladonema californicum medusae to regain pre-starvation values for biomass and metabolic rates Size group Weeks Size C N Respiration Small 1 a a a Medium 1 a a a Large NA NA NA NA 3 NA NA NA NA a Size did not decline below pre-starvation levels. NA Not available, pre-starvation levels were not reached within the 7 day renewed feeding period. scyphomedusa Aurelia aurita for intervals up to 40 days prior to renewed feeding and demonstrated that subsequent regrowth appeared morphologically identical to normal growth sequences. Likewise, C. californicum appeared to have normal tentacle, gonad and bell growth during renewed feeding experiments. One pattern which appears to be unique to C. californicum is the relationship between bell diameter and biomass during starvation. The scyphomedusa A. aurita decreased bell diameter soon after starvation, and, similarly to A. californicum, large A. aurita medusae resorbed their tissues (termed degrowth by Hamner and Jenssen, 1974) more rapidly than did small medusae. Bell diameter of the leptomedusan Aequorea victoria decreased within 2 days of starvation (Arai, 1986). In contrast, the average diameter of small and medium sized groups of C. californicum did not decline below pre-starvation levels and the large group showed only a modest decrease in diameter over 28 days of starvation. Concurrent decreases in biomass indicate that size maintenance occurred at the expense of maintaining C concentration within medusan tissues. Because hydromedusae typically lack developed lipid reserves to draw upon during starvation (as evidenced by low C:N body ratios of C. californicum, but see Larson and Harbison, 1989 for exceptions in other, gelatinous zooplankton), this implies that other tissues must have been sacrificed in order to increase or maintain bell diameter during starvation. Reallocation of biomass between different tissue types has been documented previously in other medusae. Striated muscle cells of the anthomedusa Podocoryne carnea were observed to dedifferentiate, proliferate and form 6 8 new non-muscle cell types, including nerve cells and nematocysts (termed transdifferentiation by Schmid et al., 1988; Schmid and Plickert, 1990; reviewed in Schmid, 1992). Transdifferentiation of striated muscle cells was also found in the genera Stomotoca and Polyorchis and may be a widespread ability among the hydromedusae (Schmid et al., 1988). The potential for transdifferentiation of medusan striated muscle confers on these hydromedusae considerable flexibility in allocation of cellular material to various tissues. The medusa of Turritopsis nutricula exhibits the most flexible potential for cellular transformation

13 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) Fig. 8. Comparison of bell diameter and carbon content of Cladonema californicum medusae subject to renewed feeding following a period of starvation. These data are the same as those in Figs. 6 and 7, but plotted with reference to their actual sample dates during the time course of starvation. Renewed feeding trials were initiated after 1, 2 and 3 weeks of starvation. Each renewed feeding trial lasted seven days. Sampling occurred at the outset of renewed feeding and after 1, 3 and 7 days. Clear symbols represent average diameter; filled symbols represent average carbon content per medusae. Asterisks denote sample dates on which average values were significantly different than on previous sample dates (Tukey s HSD, p,0.05). documented in the animal kingdom; fully mature medusae are capable of transdifferentiating into the polyp form under a variety of environmental conditions, including starvation (Piraino et al., 1996). Therefore, whereas reallocation of biomass between tissues of starving C. californicum medusae is a previously undescribed phenomena, the cellular processes enabling this phenomena have been well documented for other hydromedusae. Although the proximate mechanisms of diameter conservation by starving C. californicum medusae may be explained by transdifferentiation and reallocation of cellular materials during periods of declining body mass, there is less information to

14 26 J. Costello / J. Exp. Mar. Biol. Ecol. 225 (1998) explain the ultimate evolutionary forces favoring this phenomena. Both A. aurita and A. victoria decreased bell diameter rapidly during starvation, so bell diameter maintenance by C. californicum appears to be unusual among medusae. The different starvation responses of these species may be related to their foraging modes (Costello, 1992). C. californicum is an ambush predator; it sits and waits for prey to encounter its tentacles. Swimming is not an essential component of its feeding. In contrast, A. aurita and A. victoria spend a large portion of their time swimming with tentacles extended. For these predators, fluid motions created while swimming significantly affect prey capture (Costello and Colin, 1994, 1995). Swimming ability, and therefore feeding efficacy, of these cruising predators depends upon contraction of striated muscle cells during the bell pulsation cycle. The shrinking response of cruising medusan predators may permit maintenance of muscular tissues affecting swimming performance. Alternatively, the organic dilution which characterizes C. californicum s starvation response permits increased encounter radius, an important parameter in feeding success of ambush predators in general (Gerritsen and Strickler, 1977) and C. californicum in particular, because ingestion rate increases with bell diameter (Costello, 1988). Starved C. californicum swim noticeably less effectively than fed individuals, yet feed very effectively (Costello, 1988). Therefore, the starvation response of C. californicum may be a metabolic correlate of its foraging strategy. Although the starvation response patterns of only a few medusae have been studied, it is apparent that many hydromedusae are ambush predators (Mills, 1981; Arkett, 1984; Madin, 1988; Larson et al., 1991) and may share elements of C. californicum s starvation response. Maintenance of bell diameter size by C. californicum during starvation is one example among a wide range of medusan adaptations to environmental stress. Historically, the benthic polyp stage of bipartite hydromedusan life cycles such as that of C. californicum has been considered to be the most tolerant to adverse environmental conditions (Edwards, 1973; Calder, 1990; Petersen, 1990; Boero et al., 1992). Adverse conditions are survived by a long-lived polyp which can exist in an almost quiescent stage until food becomes sufficiently plentiful to support the medusa stage. The starvation response of C. californicum demonstrates that adaptations for survival of adverse environmental conditions are not limited to the polyp phase of the alternating life cycle. Other types of responses include diameter declines during degrowth (Hamner and Jenssen, 1974; Arai, 1986), direct fission (Stretch and King, 1980) and transformation to the polyp stage (Piraino et al., 1996). The considerable physiological and morphological flexibility of these medusae may be an important reason for the evolutionary success of this phylogenetically ancient group. Acknowledgements I thank P.M. Kremer and R.E. Pieper for support (NSF OCE to P.M.K. and OCE to R.E.P.) during portions of this research. Data analysis and manuscript preparation were performed while supported by NSF OCE; to J.H.C..

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