Biol. Bull. 216: 85-93. (February 2009)
© 2009 Marine Biological Laboratory
Diel Variation in the Sizes of Larvae of Bugula neritina in Field Populations
Ellen T. Kosman* and
Bruno Pernet
Department of Biological Sciences, California State University, Long Beach, 1250 Bellflower Blvd, Long Beach, California 90840
* To whom correspondence should be addressed. E-mail: etkosman{at}yahoo.com
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Abstract
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Abstract. The scale of planktonic larval dispersal affects a variety of ecological and evolutionary processes. Recent work suggests that the dispersal ability of obligately lecithotrophic larvae is influenced by the amount of energy supplied to each larva: larger larvae may stay in the plankton longer and thus travel greater distances than smaller larvae. We examined a prediction of this hypothesis in the bryozoan Bugula neritina, which each morning releases brooded larvae that settle within a few hours. If larger larvae stay in the plankton longer than smaller larvae, than larger larvae should increase in frequency in the planktonic population as the day progresses. However, field surveys revealed a negative relationship between time of day and the sizes of planktonic larvae. Because these results may have been complicated by prolonged larval release, we sequestered groups of brooding colonies in field mesocosms to examine release patterns. Larvae were released over a period of 8–9 h, with smaller larvae increasing in frequency as the day progressed. We conclude that populations of larvae of B. neritina may not be homogenous in energetic content throughout the day; this must be taken into consideration when designing studies of many aspects of larval biology.
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Introduction
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In the many species of benthic marine animals that are sessile or nearly sessile as adults, dispersal via the planktonic larval stage is one of the main determinants of demographic and genetic connectivity among geographically separated populations. Brief planktonic periods should lead to limited larval dispersal, resulting in demographic and genetic isolation of populations on small spatial scales, whereas long planktonic periods should lead to connectivity among geographically distant populations. A large body of evidence supports these general predictions (Palumbi, 1995; Bohonak, 1999; Shanks et al., 2003; Paulay and Meyer, 2006), though recent studies of some marine animals have shown or implied more restricted dispersal than predicted from the estimated duration of planktonic larval stages (Jones et al., 2005; Cowen et al., 2006; Gerlach et al., 2007; Teske et al., 2007). Because dispersal by larvae has critical effects on these ecological and evolutionary processes, it is important to understand the factors that govern its scale. One such factor is the amount of energy that larvae are provisioned with by their parents.
Larval energetic resources, both endogenous and exogenous, have often been linked to planktonic duration and, often indirectly, to dispersal ability (Vance, 1973; Strathmann, 1985; Levitan, 2000). In broad interspecific comparisons involving species with both planktotrophic (feeding) and obligately lecithotrophic (nonfeeding) larvae, greater amounts of energy invested per offspring are associated with shorter planktonic durations (Levitan, 2000; Shanks et al., 2003) and reduced dispersal (Palumbi, 1995; Bohonak, 1999). Planktotrophic larvae have relatively few maternally derived energy reserves but have the ability to capture and ingest particles, so there is no obvious energetic upper limit on the amount of time these larvae spend in the plankton. In contrast, the dispersal ability of obligately lecithotrophic larvae is limited by their endogenous energy reserves (Jaeckle, 1995). The only potential exogenous source of energy for such larvae is the uptake of dissolved organic material, but it is unclear how effective this is in prolonging planktonic duration (Jaeckle, 1994; Wendt and Johnson, 2006). Therefore, for obligately lecithotrophic larvae, one might expect to find a positive relationship between the quantity of endogenous energy reserves and potential planktonic duration.
Such a relationship is apparent in comparisons among some closely related species of bryozoans; here, the larger larvae of some species retain metamorphic competence longer than do the smaller larvae of other species (Wendt, 2000). Because per-offspring energetic investment (often estimated as offspring size) may also be quite variable within species (Isomura and Nishihira, 2001; Marshall and Keough, 2008a), such correlations may also be evident in intraspecific comparisons. In a laboratory study that made intraspecific comparisons of the behavior of lecithotrophic larvae, Marshall and Keough (2003) showed that large larvae of the ascidian Diplosoma listerianum and of two bryozoans (Bugula neritina and Watersipora subtorquata) swam for longer than did smaller larvae of the same species. Those authors also compared the sizes of settlers in a field population of W. subtorquata in the morning and afternoon, finding that individuals that settled in the afternoon were larger than those that settled in the morning. Together these results are consistent with the hypothesis that large larvae may remain in the water column for longer than small larvae; this longer planktonic period may then allow larger larvae to disperse farther than smaller larvae.
In this study, our initial goal was to test the hypothesis that larger larvae remain in the plankton longer than do smaller larvae in natural populations of Bugula neritina (Linnaeus, 1758). Mature colonies of this bryozoan release larvae daily at dawn, and the larvae settle within a few hours (Ryland, 1974; Wendt, 2000). Larvae vary greatly in size both within colonies and within populations (from 
250–320 µm in diameter: Marshall and Keough, 2006; Kosman, unpubl. data). Interspecific comparisons within the genus Bugula show that larval size is correlated with larval energetic content (Wendt, 2000). It seems likely that this also holds at the intraspecific level, as suggested by the correlation of larval size with several aspects of post-metamorphic performance in B. neritina (Marshall et al., 2003; Marshall and Keough, 2004). Colonies are often abundant on docks and piers and can release tens to hundreds of larvae each day (Mawatari, 1951). Natural variability in per-offspring investment, high adult densities, and daily larval release make B. neritina an excellent model system for analyses of cohorts of planktonic larvae. If our hypothesis was correct, we predicted that sampling cohorts of planktonic larvae throughout the day should yield evidence of increased dominance of larger larvae as the day progressed.
This prediction relies on the assumption that patterns of larval release in the field are similar to those observed in isolated colonies in the laboratory, where most larvae are released in a discrete burst on exposure to light. A second goal of our study was to test this assumption by repeatedly sampling field mesocosms containing adult colonies for released larvae, and examining the number and sizes of larvae released in each sampling period.
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Materials and Methods
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We tested the hypothesis that larval size affected planktonic duration by conducting surface plankton tows hourly throughout the day at two sites in Alamitos Bay, Long Beach, California. All surveys were carried out during neap tide series on days chosen to minimize tidal currents. On 24 and 25 September 2005, tows were done from 0600 to 1700 from a dock bisecting Colorado Lagoon (33°46.251'N, 118°08.090'W). The population of adult Bugula neritina at this site was almost exclusively located on the dock, as indicated by subtidal surveys that suggested that there were few other hard surfaces in the lagoon suitable for bryozoan colonies (Chambers Group, 2004). Preliminary surveys showed that very few larvae were present in the plankton before sunrise or after 1700. While walking the length of the dock four times (a total of 133 m), we towed a plankton net with an opening diameter of 32 cm and a mesh size of 80 µm. On 24 July 2007 we performed hourly surface tows at a second site, a dock in Alamitos Bay Marina (33°45.189'N, 118°06.689'W), from 0700 till 1500. Because this dock was very short (3 m) and larvae of B. neritina were generally less abundant than at Colorado Lagoon, we walked back and forth along the dock until at least 10 larvae were captured, this time using a plankton net with an opening diameter of 21 cm and a mesh size of 53 µm. The focal dock at this site was surrounded by many other docks that also bore dense populations of B. neritina. We were constrained to sampling via surface tows because both sites were shallow (maximum depth 3 m at Colorado Lagoon and 4 m at Alamitos Bay Marina) and sampling sufficient larvae across depths with a plankton net would have taken too long for each sample. However, given the shallow depths and the fact that some current-induced vertical mixing was certainly occurring, we felt that our surface tows likely collected an unbiased sample of the larval population at each site.
Plankton samples were immediately preserved in 4% formalin in seawater. Almost all bryozoan larvae in samples were those of Bugula neritina and were easy to distinguish from those of other bryozoans (mainly Bugula californica). From each sample that contained sufficient larvae, 20 larvae of B. neritina were haphazardly selected, mounted on slides with coverslips supported at their corners with modeling clay so as not to compress larvae, oriented with the ciliated groove upward, and photographed with a compound microscope. If there were fewer than 20 larvae in the sample, as was generally the case at Alamitos Bay Marina, then all larvae in the sample were photographed. The length (parallel to the ciliated groove) and diameter (perpendicular) of each larva was measured from the photographs using ImageJ 1.34s (Abramoff et al., 2004). These measurements were then used to estimate larval volume, with the simplifying assumption that larvae were cylindrical (Wendt, 2000; Marshall et al., 2003). In a preliminary study, the sizes of fixed larvae were found to be reliable indicators of the sizes of living larvae (Kosman, unpubl. data). To determine whether time of day was related to the sizes of larvae present in the plankton, we used analysis of covariance (ANCOVA) with day as a random factor and time as a covariate. Residuals were examined graphically to ensure conformity with ANCOVA assumptions. To test for heterogeneity among slopes, we examined the interactions between day and time. As no significant interaction was detected, a post hoc Tukey's test was used to identify differences in the mean larval volumes released among the days.
Because larvae present in the plankton later in the day may have been swimming for several hours, they might have become smaller during the course of the day as they depleted their energy stores. We looked for this effect in a laboratory experiment. Adult colonies gathered from Colorado Lagoon from May to July 2006 were held for 24 h in a darkened flow-through aquarium, and then induced to release larvae by exposing the dark-adapted colonies to a bright light. Thirty-three larvae were individually mounted on slides with supported coverslips and videotaped with a compound microscope. For each larva, a single video frame with the larvae in the correct orientation (ciliated groove upward) was extracted and used to estimate larval volume as above. To prevent settlement, the larvae were then placed individually in 1.5-ml microcentrifuge tubes on a gently shaking orbital shaker—a modification of the technique of Hunter et al. (1999)—for 8 h. We checked larvae periodically during the 8-h period, gently pipeting the water in each tube to provide additional agitation to prevent settlement. After swimming for 8 h, the larvae were videotaped and measured again, and larval volume estimates before and after swimming were compared with a paired Student's t-test.
Our initial prediction relied on the assumptions that in the field, all larvae are released in a single discrete burst soon after dawn, or if larval release is prolonged over several hours, that the sizes of larvae released do not change over the period of larval release. To test these assumptions, we sequestered adult colonies in field mesocosms and sampled released larvae hourly throughout the day. We constructed rectangular clear acrylic boxes (20 x 40 x 10 cm) open at one end, suspending these lengthwise from the side of a dock, so that most of each box was submerged. Circulation through each box was allowed through two holes (15 x 5 cm) in its sides; holes were covered with 65-µm mesh to retain released larvae. Six boxes were deployed from the side of the dock at Colorado Lagoon on 14 June 2007, and five boxes were similarly deployed at Alamitos Bay Marina on 24 July 2007. Light intensities inside the deployed boxes were measured with a Li-Cor LI185B photometer with a 3D underwater light sensor and were found to be similar to the conditions in the water immediately adjacent to the boxes.
Before sunrise on each day, we collected colonies from the dock immediately adjacent to where the boxes were mounted, and placed three colonies of about the same size into each box, mounting them on clips attached to the walls of the boxes so as to maintain their original depth and orientation. Including multiple parent colonies in each box was necessary so that enough larvae would be released at each time period. At Alamitos Bay Marina, the dry weights of the colonies placed in the boxes ranged from 1.40 to 2.01 g. Colonies placed in the boxes at Colorado Lagoon were not weighed, but were larger than those used at Alamitos Bay Marina. We used a portable bilge pump to pump about 12 l of seawater from each box every hour from 0600 until 1500; pumped water was passed through a 65-µm mesh to capture all released larvae. Preliminary laboratory tests showed that this method of sampling captured all larvae in the box, though 5% of captured larvae were damaged in the process; and a field experiment showed that no larvae from outside the boxes were forced through the box mesh as the box refilled during the pumping process (Kosman, unpubl. data).
The number of larvae in each sample was recorded, and 20 larvae were haphazardly selected from each sample and photographed. All captured larvae were photographed if fewer than 20 larvae were released into a box at a given sampling time. Larval volumes were estimated from the photographs as described above. Larvae damaged in collection were included in counts but excluded from volume analyses. A two-factor ANCOVA was performed with site and box included as random main effects (box nested within site) and time as a covariate. Residuals were examined graphically to ensure conformity with ANCOVA assumptions. To test for heterogeneity among slopes, we examined interactions between the main effects and time. When an interaction was found, we calculated the coefficients for each of the main effects and determined significance using a Bonferroni-corrected alpha value. Significant coefficients were used to identify differences among the slopes. Boxes with differing slopes were removed from the model, and a reduced ANCOVA with site and box as main effects (box nested within site) and time as a covariate was run.
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Results
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Planktonic larvae of Bugula neritina varied in volume up to about 4-fold on each of the three sampling dates (Fig. 1). There was a significant effect of both day and time on the volumes of larvae present in the plankton, but no interaction between day and time (Table 1). On average, larvae found in the plankton on 24 July 2007 were significantly larger than those found on 24 and 25 September 2005 (F = 4.85, P = 0.008). The mean volume of larvae released on 24 July 2007 was 0.0151 ± 0.0002 mm3, while those released on 24 and 25 September 2005 averaged 0.0133 ± 0.0002 mm3 and 0.0129 ± 0.0002 mm3, respectively (±one standard error, SE). On all three sampling dates, there was a significant negative relationship between time and larval volume, with smaller larvae becoming more prevalent in the plankton later in the day (Fig. 1).
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Figure 1. Volumes of larvae of Bugula neritina found in plankton tows on three sampling dates. There were significant negative relationships between sizes of larvae present in the plankton and time of day on all three dates. Larger larvae were found in the 2007 tows (C), and smaller larvae found in the 2005 tows (A and B).
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Table 1 Results of an ANCOVA analysis of the sizes (as volume) of larvae of Bugula neritina found in hourly plankton tows on three sampling dates, with day as a random factor and time as a covariate
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In the laboratory, 8 h of forced swimming had no effect on larval volume (paired t-test, t = –1.25, n = 33, P = 0.219). Mean larval volume prior to swimming was 0.0089 ± 0.0028 mm3, and after 8 h of swimming it was 0.0092 ± 0.0027 mm3 (mean values ± SE). Post hoc power analysis showed that at a power of 99%, this test should have been able to detect a change in larval volume of 0.0009 mm3 (10% of initial volume; Quinn and Keough, 2002). Observed declines in mean larval volume over 8 h in planktonic populations at Colorado Lagoon were 0.0020–0.0030 mm3 (14%–20% of initial volume; Fig. 1).
Sampling of larvae from field mesocosms revealed that larval release was prolonged, lasting from 8 to 9 h a day. Appreciable numbers of larvae first appeared in the boxes at 0700, about an hour after sunrise, and larval release continued until 1500 (Fig. 2). Peak larval release occurred from 0800 to 1200 at Colorado Lagoon, and 0800 to 1100 at Alamitos Bay Marina. In the boxes at Colorado Lagoon, 50% of the total number of larvae released were released by the 1100 sampling, and at Alamitos Bay Marina, by the 1000 sampling. The smaller Alamitos Bay Marina colonies produced fewer larvae than those from Colorado Lagoon. Groups of colonies sequestered in the boxes at Colorado Lagoon released well over 30 larvae during each peak release hour, while those sequestered in Alamitos Bay Marina generally released 15 or fewer larvae each hour (Fig. 2).
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Figure 2. Numbers of larvae released each hour from colonies sequestered in field mesocosms at Colorado Lagoon (n = 6) and Alamitos Bay Marina (n = 5). Error bars are + one standard deviation.
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There was no effect of site on the volumes of larvae released in the boxes; however, there was heterogeneity among the slopes as indicated by the significant interactions between site and time, and box and time (Table 2). In Colorado Lagoon, the interaction between box and time was due to Box 1, which had a significantly steeper slope than the other five boxes (Fig. 3: b = –0.0268, P < 0.001). There was no difference among the slopes of the other boxes within Colorado Lagoon. In Alamitos Bay Marina, the interaction between box and time was due to Box 3, whose slope was not significantly different from zero (Fig. 4: b < 0.0001, P = 0.394). There were no differences among the slopes of the other four boxes within Alamitos Bay Marina.
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Table 2 Results of an ANCOVA analysis of the sizes (as volume) of larvae of Bugula neritina found in hourly samples taken from field mesocosms (boxes), with site and box (nested within site) as random factors and time as a covariate
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Figure 3. Scatterplots with ordinary least square regression lines showing relationships between larval volume and time of release by adult colonies in each of the six field mesocosms (boxes) at Colorado Lagoon. There were significant negative relationships between larval volume and time of release in all boxes. Box 1 had a significantly steeper slope than the other five boxes (b = –0.0268, P <0.001).
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Figure 4. Scatterplots with ordinary least square regression lines showing relationships between larval volume and time of release by adult colonies in each of the five field mesocosms (boxes) at Alamitos Bay Marina. There were significant negative relationships between larval volume and time of release in four of the five boxes. Box 3 had a slope significantly different from those the other four boxes, but not significantly different from zero (b <0.0001, P = 0.394).
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When Box 1 from Colorado Lagoon and Box 3 from Alamitos Bay Marina were removed from the analysis, there were no longer interactions between site and time, or box and time (Table 2). Additionally, there was no difference in the mean volume of larvae released between sites or among boxes within sites. However, there was still a significant negative relationship between time and the volumes of larvae released (b = –0.0157, P < 0.001).
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Discussion
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Our initial prediction, based on Marshall and Keough's (2003) laboratory results showing that larger larvae spend more time in the plankton than smaller larvae, was that larger larvae of Bugula neritina would increase in frequency in the planktonic population over the course of the day. However, we found the opposite: in each of 3 days of sampling, smaller larvae of B. neritina increased in frequency in plankton samples as the day progressed (Fig. 1).
A variety of processes might partly or completely explain these observed temporal patterns in size structure in planktonic populations. One possibility is that larvae shrink as they expend energy. Because some larvae present later in the day may have experienced several hours of swimming, and because swimming has an energetic cost, the depletion of energy reserves might lead to a decrease in size. However, we observed no decrease in larval size in the laboratory after 8 h of forced swimming. Further, Hunter et al. (1998) showed that larvae of Bugula neritina did not shrink after swimming for up to 24 h. As the larvae we sampled in the plankton swam for 9 h at most, it seems very unlikely that individual larvae sampled later in the day had shrunk due to energy depletion over the course of the day.
Another possibility is that the temporal patterns observed in larval size structure were due to behavioral differences between small and large larvae. For example, larger larvae might have dispersed or settled more rapidly than smaller larvae, leaving the smaller larvae to make up a higher proportion of the planktonic population later in the day. We are aware of only a few studies that compare larval swimming speed among ciliated larvae of similar stages but different sizes, and these do not suggest that larger larvae swim faster than smaller larvae (Wendt, 2000; McDonald, 2004). Marshall and Keough (2003) have described differences in settlement behavior between small and large Bugula neritina; however, they showed that smaller larvae settled sooner than larger larvae, whether or not settlement cues were present in the laboratory. No work to date has compared the behaviors of small and large larvae of B. neritina in the plankton, so we cannot rule out the possibility that members of these two classes of larvae differ in their vertical positioning or phototactic behaviors, or in other behaviors that might affect dispersal. However, it is worth noting that size-specific behavioral differences cannot explain the similar pattern (smaller larvae increasing in frequency as the day progressed) we observed in the mesocosms, as those larvae were captured very soon after release and had no chance to disperse and little opportunity to settle.
The patterns we observed may also have been due to the gradual immigration of larvae released from other populations. There are many reports of spatial variation in the sizes of eggs or embryos produced by marine invertebrates, including bryozoans (Jones et al., 1996; George, 1999; Phillips, 2007; Marshall and Keough, 2008b). Smaller larvae produced in spatially isolated benthic populations might have immigrated toward the focal docks, showing up in plankton tows later in the day. This is unlikely to be the case at Colorado Lagoon, where most of the adult population was located at the focal dock. However, the possibility that smaller larvae immigrating from other source populations contributed to the pattern observed in the plankton cannot be ruled out completely, especially for the Alamitos Bay Marina site, where the focal dock was surrounded by other docks that also bore dense populations of B. neritina. As above, however, it is worth noting that immigration cannot explain the similar patterns that we found in mesocosms, where there were no potentially confounding effects of other source populations.
The simplest explanation for the temporal patterns that we observed in size structure of planktonic larval populations is that they reflect temporal patterns in the sizes of larvae released by benthic colonies. We found that groups of colonies in field mesocosms released larvae over 8–9 h of each day (Fig. 2), not in a discrete burst early in the morning, and that the average sizes of larvae released declined as the day progressed (Figs. 3, 4). This decline in the sizes of larvae released over the course of the day was very similar to that seen in the sizes of larvae present in the planktonic population, raising the possibility that the dynamics of larval release had a strong effect on the size structure of the planktonic population.
On initial viewing, our data on the planktonic larvae of B. neritina seem inconsistent with the previous observations of Marshall and Keough (2003) on another bryozoan, Watersipora subtorquata. In laboratory experiments they found that larger larvae of this species (and of B. neritina) stayed in the water column longer than did smaller conspecific larvae, and in field experiments they found that juvenile W. subtorquata that metamorphosed later in the day were larger than those that metamorphosed earlier in the day. For W. subtorquata, at least, these results suggest that larger larvae should dominate in the plankton later in the day. We found the opposite pattern—increasing dominance of smaller larvae in the plankton later in the day—in two Alamitos Bay populations of B. neritina. However, more data are needed to determine whether these results are actually inconsistent. It is possible, for example, that the dynamics of larval release differ between the two species, with W. subtorquata releasing all larvae in a burst early in the morning, in contrast to the prolonged, size-structured larval release that we observed in B. neritina. Another possibility is that the smaller larvae of B. neritina present later in the day in Alamitos Bay populations are less capable of successful metamorphosis than larger larvae, so that an experiment looking at the effects of time of day on the sizes of settling juveniles might yield results similar to those of Marshall and Keough (2003) on W. subtorquata. Further work that simultaneously examines the dynamics of size structure during all three processes—larval release, planktonic dispersal, and settlement—in a single species would be very useful.
The mesocosm results showing that larval release occurred over many hours throughout the day were consistent with the only (to our knowledge) previous studies of larval release under somewhat naturalistic conditions (Cancino et al., 1991, 1992, 2002). These results did contrast with the pattern commonly reported in the laboratory, a discrete burst of larval release at first light. Most laboratory studies of bryozoan larvae expose dark-adapted colonies to sudden high-intensity light to stimulate release within 1 to 2 h (Wendt, 2000; Marshall and Keough, 2003). In nature, the onset of solar illumination is rather gradual, and the initial intensity of light is lower than that in the laboratory. Our results and those of Cancino et al. (1991, 1992, 2002) suggest that prolonged larval release may be a common pattern in natural populations of bryozoans. Unfortunately, we cannot distinguish between the hypotheses that prolonged release of larvae occurs at the individual (within-colony) level or at the population (among-colony) level, because in all of these studies the investigators included multiple adult source colonies in each mesocosm.
The mechanisms underlying this gradual release of larvae are not known. Among the many possible explanations for this phenomenon, perhaps the simplest are related to spatiotemporal variation in the intensity of the cues for larval release, or in responsiveness to the cues. It is clear that light plays a major role in inducing larval release in many bryozoans, though few details of this process are known (Mawatari, 1951; Ryland, 1974; Cancino et al., 1991, 1992, 2002). If light of a minimum threshold intensity is required to stimulate larval release from each brooding zooid, then perhaps that threshold is not reached simultaneously at all brooding zooids in the field. For example, soon after sunrise, zooids on the exterior branches of colonies of B. neritina may receive sufficient light to be stimulated to release larvae. However, zooids shaded by other branches of the same colony, by neighboring colonies, or by other structures, may not experience light of sufficient intensity until later in the day, resulting in prolonged larval release at the population level. One might expect that the effects of such "same-colony" or "neighboring-colony" shading on the timing of larval release might vary depending on colony morphology (for example, zooids in encrusting colonies may experience less variability in light stimuli than zooids in structurally complex branching colonies). In addition, zooids that are brooding larvae may be variably sensitive to light cues (perhaps as a function of the developmental stage of the brooded embryo), again leading to possible temporal variation in the timing of larval release.
Our finding that larvae released later in the day were smaller than those released earlier in the day is novel. It is well known from previous studies that bryzoan larvae vary greatly in size both within and among colonies at a site (Marshall and Keough, 2008b; Kosman, unpubl. data). What remains a puzzle is why larvae of different sizes appear to be released at different times (at least at the population level; again, because we included multiple source colonies in each mesocosm, we cannot distinguish between the hypotheses that the mesocosm-level temporal patterns in larval size structure were caused by variation in the sizes of larvae released at the individual colony level or at the population level. This is a question that merits further work). One possibility is that the observed variability in larval size is partly due to among-zooid differences in the ability to capture food and thus provision developing embryos. Zooids in the interior of colonies of B. neritina may experience a poorer feeding environment than do exterior zooids, and thus might produce smaller larvae, if exterior zooids disrupt the flow of water currents or deplete food in those currents (Okamura, 1985). Such a mechanism might also operate at the population level, if some colonies obtain less food because of flow disruption or food depletion by neighboring colonies (Buss and Jackson, 1981; Okamura, 1985, 1992). As noted above, zooid placement or colony density might also explain prolonged larval release in field populations, as shaded zooids or colonies may not be stimulated by light of sufficient intensity until later in the day. If internal zooids or crowded colonies produce smaller larvae and are also shaded by exterior zooids or neighboring colonies, we might expect to see a link between larval size and the time of release, with smaller larvae being released later in the day.
Overall, our results strongly support Marshall and Keough's (2003) argument that lecithotrophic bryozoan larvae in planktonic populations are heterogeneous in size and behavior throughout the day. As previously described, larvae released by Bugula neritina and other bryozoans are highly variable in size (reviewed by Marshall and Keough, 2008a). Complicating this further, we have shown that there are distinct temporal patterns in the sizes of larvae of B. neritina released and present in the plankton. Larval size may be related to energy content (Wendt, 2000), and size frequently has strong effects on larval, juvenile, and even adult performance (Marshall et al., 2003; Marshall and Keough, 2004, 2008b). At any given time, then, populations of planktonic larvae of B. neritina (and perhaps other bryozoans) are highly heterogeneous in this important trait, and the quality of this heterogeneity varies throughout the day. Such patterns must be taken into account when designing or interpreting observations or experiments on almost any aspect of larval or juvenile performance.
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Acknowledgments
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The authors thank L. Mastro and K. Anthony for the use of equipment, C. Tenorio for assistance in the field, and E. Fernandez-Juricic and J. Archie for statistical advice. We thank two anonymous reviewers for comments that improved an earlier version of this manuscript. Support was provided by a Grant in Aid of Research from the Society for Integrative and Comparative Biology (to E.K.), a Southern California Tuna Club Marine Biology Foundation Scholarship (to E.K.), and by the Department of Biological Sciences and the College of Natural Sciences and Mathematics at CSU Long Beach.
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Footnotes
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Received 30 May 2008; accepted 30 October 2008.
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Abstract
Introduction
