Biol. Bull. 202: 156-165. (April 2002)
© 2002 Marine Biological Laboratory
Variation in Growth and Competitive Ability Between Sexually and Clonally Produced Hydroids
David H. Van Winkle* and
Neil W. Blackstone
Department of Biological Sciences, Northern Illinois University, DeKalb, Illinois 60115
* To whom correspondence should be addressed. E-mail: rip{at}niu.edu
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Abstract
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In controlled laboratory experiments, colonies of Podocoryna carnea typically overgrow and kill colonies of Hydractinia symbiolongicarpus. Generally, these experiments have used colonies grown from tissue explants (clonal replicates) surgically removed from mature colonies taken from natural populations. In contrast, experiments involving interspecific bouts between small, sexually produced colonies reveal that both the characteristics and outcomes of competition differ from previous studies. During competition between small sexually produced colonies, H. symbiolongicarpus exhibits directional growth toward P. carnea and produces nematocyte-rich hyperplastic stolons more readily than P. carnea does. Nevertheless, P. carnea can still overcome H. symbiolongicarpus if it initially grows away from the contact zone and subsequently flanks H. symbiolongicarpus. Overall, sexually produced colonies of H. symbiolongicarpus destroyed their P. carnea counterparts in more than 35% of competitive bouts, whereas P. carnea dominated their H. symbiolongicarpus counterparts in all similar encounters between clonally produced colonies. In natural populations, competition between small sexually produced colonies of H. symbiolongicarpus may predominate, and these results support the hypothesis that this species is adapted to competition early in colony development. More generally, studies of competition between sexually produced colonies should complement similar studies of clonally produced colonies.
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Introduction
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Colonial animals can be described morphologically as a collection of iterated modules or ramets interconnected by a common vascular network. The arrangement of modules and vascular connections defines two contrasting colonial morphologies and associated life histories (e.g., Larwood and Rosen, 1979; Jackson et al., 1985; Buss and Blackstone, 1991). Briefly, "sheets" exhibit a robust morphology, having tightly packed modules interconnected by short vascular stolons. Specialized to particular habitats, sheets are typically good competitors and persistent over time. In contrast, "runners" tend to have a haphazard distribution of modules, and they are typically transient generalists that are competitively inferior to sheets but can potentially escape competitive encounters through copious asexual or sexual propagation. Within these extremes, many colonial organisms display varying degrees of morphological plasticity in response to environmental conditions, which probably enables them to adapt to heterogenous environments (e.g., de Kroon and Hutchings, 1995; Umeki, 1995; Stuefer, 1996; Kleijn and Van Groenendael, 1999; Muko et al., 2000; Equiza et al., 2001).
The colonial hydroids Podocoryna carnea and Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa) occur sympatrically. Both encrust gastropod shells of paguriid hermit crabs in North American nearshore waters of the Atlantic Ocean. Although genotypic and phenotypic variation does occur, each is more or less representative of the extremes of the classic runner-sheet dichotomy. Specifically, P. carnea is runner-like and H. symbiolongicarpus is sheet-like (e.g., McFadden, 1986; Blackstone and Buss, 1991; Buss and Blackstone, 1991; Van Winkle et al., 2000). The former has sparse, unevenly spaced modules, whereas the latter develops a tight network of evenly spaced modules and grows over available space more slowly. Additionally, the ectoderm fuses between stolons of H. symbiolongicarpus within 2 weeks after metamorphosis from planula larvae. This stolonal "mat" (Hauenschild, 1954, 1956) expands from the colony’s center to encompass existing peripheral stolons and slowly deposits a thick, chitin-like understory, which markedly increases the sheet-like appearance of these colonies.
Although H. symbiolongicarpus and P. carnea display contrasting life-history characteristics consistent with runner and sheet generalizations, such is not the case with competitive ability. Previous work using clonally produced colonies has shown that P. carnea is almost invariably the competitive dominant to H. symbiolongicarpus under laboratory conditions (McFadden, 1986; Van Winkle et al., 2000). Additionally, P. carnea covers available space faster and responds more aggressively to foreign tissue (Tardent and Bührer, 1982; Buss et al., 1984; McFadden et al., 1984; McFadden, 1986; Lange et al., 1992; Van Winkle et al., 2000). A unique aspect of cnidarian biology can explain these disparities: competition in hydroids is mediated by cnidarian-specific cells (nematocytes) actively deployed from hyperplastic stolons. These specialized stolons develop only from previously existing stolons or from a particular type of mat tissue termed astogenetic mat (Buss and Grosberg, 1990), and they represent an example of an inducible defense (c.f., Frank, 1993; Harvell, 1990). Thus, competitive ability in hydroids is largely determined by colony morphology, and runner-like colonies have consistently been shown to be superior competitors, presumably due to their extensive peripheral stolons (McFadden et al., 1984; Buss and Grosberg, 1990; Yund, 1991).
Regardless of its competitive inferiority, H. symbiolongicarpus is far more abundant than its competitor on small gastropod shells occupied by Pagurus longicarpus (Yund et al., 1987; Buss and Yund, 1988; Yund and Parker, 1989), and colonies eventually cover the entire shell surface, thus excluding further larval recruitment. Although P. carnea can be found on small, rough-surfaced shells (e.g., Nassarius trivittatus) amidst shells covered by the more common H. symbiolongicarpus, these colonies are small, rarely covering the shell surface entirely (Buss and Yund, 1988). In natural populations of H. symbiolongicarpus, competition is probably more common among small, newly established colonies shortly after the metamorphosis of larvae generated by sexual reproduction than among older, well-established colonies (Yund et al., 1987). Thus, competitive encounters among young, sexually produced hydroid colonies in nature and those experimentally induced among clones of unknown age may be qualitatively different. Nevertheless, studies of both intraspecific and interspecific competition in these hydroids have been limited exclusively to clonal replicates usually taken from well-established colonies of unknown age in natural populations (Hauenschild, 1954, 1956; Braverman and Schrandt, 1966; Tardent and Bührer, 1982; McFadden, 1986; Müller et al., 1987; Plickert et al., 1987; Lange et al., 1989; Buss, 1990; Buss and Grosberg, 1990; Blackstone and Buss, 1991; Yund, 1991; Grosberg et al., 1996; Van Winkle et al., 2000).
Considerable recent work regarding age-specific variation in growth, morphology, and competitive ability has focused on plants (e.g., Lundberg et al., 1996; Bertschy, 1998; Moora and Zobel, 1998), which are similar to colonial animals in developmental mode and morphology (i.e., modular organization). Colonial hydroids also seem to display age-specific differences in growth and morphology, and these differences could affect competitive ability at different stages of colony development. Clonally produced colonies (clonal replicates) of H. symbiolongicarpus exhibit important morphological and physiological differences relative to newly established (hereafter termed sexually produced) colonies. First, the development of stolonal mat is delayed for up to 2 weeks in sexually produced colonies, whereas clonally produced colonies always exhibit these mats. Second, sexually produced colonies initially produce many more peripheral stolons than clonal replicates do, and the morphological shift associated with stolonal mat formation is accompanied by a decrease in the rate of flow of gastrovascular fluid to peripheral stolon tips (Blackstone, 1996). In contrast, the flow rate to stolon tips gradually increases after metamorphosis in P. carnea (Blackstone, 1996), which tends to grow more sheet-like only after sexual maturity, never becoming as sheet-like as H. symbiolongicarpus. Due to the qualitative differences between early growth in sexually produced and clonally produced colonies, it is plausible that such colonies may also display age-specific differences in competitive ability.
We examined interspecific competition between H. symbiolongicarpus and P. carnea during early post-metamorphic development of sexually produced colonies and likewise between clonally produced colonies. We sought to characterize competitive ability in two ways. First, the outcome of single colony interspecific competition for space was determined both among F1 sexually produced colonies and among the parental clonal replicates. Second, in these interactions we characterized directional growth before and after colony interaction by using colony area and geometric center of mass. Overall growth toward a competitor may indicate a controlled and purposeful attack response, whereas overall growth away from a competitor may indicate an escape response. We found considerable variation between sexually and clonally produced colonies; thus our results complement earlier studies of competition between clonally produced colonies and perhaps suggest why H. symbiolongicarpus predominates on gastropod shells inhabited by paguriid hermit crabs.
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Materials and Methods
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Competition in sexually produced colonies
Wild-type colonies of Hydractinia symbiolongicarpus and Podocoryna carnea were maintained as described previously (Van Winkle et al., 2000). A single cross of wild-type parental colonies was used to generate F1 planula larvae of each species. We used only a single cross of each species because a broad distribution of runner- and sheet-like morphologies is represented among full siblings (Blackstone, 1996), and the crosses used produced a typical distribution of forms. Thus, broad variation in competitive ability of F1 full sibs was expected for each species.
Mature male and female colonies of each species were placed in covered glass dishes in an incubator at 20.5 °C and induced to release gametes or medusae by exposure to artificial, full-spectrum lighting following an overnight period of total darkness. Parental colonies were separated from gametes or medusae after this period. Colonies of P. carnea were induced to release medusae 3 days prior to the induced spawning of H. symbiolongicarpus gametes because the latter lack the medusoid phase and thus require less time to generate mature planulae. Medusae were fed brine shrimp and placed in fresh seawater daily during this time and for 2 days thereafter. On the 3rd, 4th, and 5th days, medusae spawned gametes, and fertilized eggs were collected and isolated in a dish containing fresh seawater. Also on the night of the 3rd day, colonies of H. symbiolongicarpus were induced to release gametes as described. On the following morning, fertilized eggs of H. symbiolongicarpus were transferred to a dish containing fresh seawater. All F1 larvae of both species were fully mature by the 9th day after medusoid release of P. carnea parental colonies. Planulae were induced to metamorphose using 50 mM CsCl in seawater for 3 h (Spindler and Müller, 1972; Blackstone, 1996). Single metamorphosing larvae of each species were randomly paired and placed about 4 mm apart near the center of 30 round (18-mm) glass coverslips in petri dishes; these were left undisturbed in total darkness for 48 h. Once attached to the glass surfaces, all newly metamorphosed primary-polyp pairs were digitally imaged, placed in floating racks in 120-1 aquaria, and hand-fed brine shrimp nauplii daily until each grew large enough to consistently capture its own food. Primary polyps of each species were easily distinguished by their appearance. Thirteen coverslips were excluded due to degeneration or the inability to feed of one primary polyp. Of the 13, 12 were excluded due to the degeneration of a P. carnea primary polyp, and one was excluded due to the degeneration of a H. symbiolongicarpus primary polyp.
Second images of the remaining colony pairs (n = 17) were captured at the time of inter-colony contact and third images at 14 d after first contact. The 14-d time interval was chosen based on previous observations of interspecific competition; that is, "snapshots" of competition were most meaningful as far along in the interaction as possible while both colonies were still alive and growing. Three of the competitive interactions were resolved (one of the pair was killed by the other) before 14-d images were captured (remaining, n = 14). All three sequential images were captured at equal magnification and orientation, such that colony spatial relationships were preserved in each image sequence.
Competition in clonally produced colonies
Tissue explants of mature, field-collected colonies were used to generate clonal replicates. These were treated identically to sexually produced colonies in all respects except for the manner in which they were initiated. Eight clonal replicates of each of the two parents of sexually produced colonies of each species were used as clonally produced colonies, yielding a total of 32 colonies and allowing four unique interspecific pairwise combinations replicated four times (n = 16). Single-polyp tissue explants were placed about 4 mm apart near the center of 18-mm round glass coverslips. Explants were held in place with nylon threads until attachment occurred, whereupon the threads were removed. Initial colony images were captured upon attachment of both colonies to the growing surface. Of the 16 colonies of H. symbiolongicarpus, 3 died prior to first contact (n = 13), and 2 were killed during competition prior to 14 days post-contact (remaining, n = 11).
Data collection and analysis
Images of all competing colonies were analyzed using Optimas 6.1 image analysis software (Media Cybernetics). From all images, geometric center of mass (hereafter termed "position") was calculated based on total area covered as measured by the outer perimeter of each colony. The outer perimeter was digitally traced according to the actual contours of the colony, not as a polygon. The resulting data were in the form of a single point in Cartesian space for each colony, where all positive x and y values numerically balanced with their corresponding -x and -y values; therefore, each point represented the overall average of two-dimensional space controlled by a colony at a given time. Overlapping areas were considered to be mutually controlled. Since the three sequential images of each bout were captured at equal magnification and orientation, relative changes in position could be followed for each species on each coverslip.
These data were analyzed in two ways. Multivariate analysis of variance (MANOVA) was used to test whether the relationship among colony positions—as given by x and y coordinates—changed between the time of contact and 14 days post-contact. Thus, MANOVA tested for a significant change in the overall relationship of four response variables (position x and y coordinates of each species) using time as a predictor. While each response variable was technically two repeated measures grouped by coverslip, it was impossible to simultaneously test four repeated response variables using time as the predictor, due to the lack of error variance in such a model. Analysis of colony position relationships prior to contact was meaningless using this method of analysis, because colonies of each species begin growth from a predefined position. Nevertheless, MANOVA provided a clear and intuitive exploratory analysis of an overall post-contact colony response. The initial distance between competing colonies varied slightly on each coverslip due to larval or explant placement error. To allow for realistic comparisons of relative changes in colony position coordinates among coverslips, the initial distances between competitor positions were adjusted to a common value equal to the average distance between primary polyps or explants among all coverslips. The remaining data were standardized proportionately to reflect these changes.
An alternate and more precise method of analysis using paired t tests was devised to determine whether relative position changed over each interval for each species. This method simultaneously accounted for the potential interdependency of within-subject colony interactions and the effects of repeated measures on the same subject (i.e., coverslip). The three images of each coverslip (primary polyps, contact, and 14 days post-contact) contained two time intervals over which colony position changed: (1) the change from initiation (positions of primary polyps or explants) to contact and (2) the change from contact to 14 days post-contact. As stated previously, the initial distance between competing colonies varied slightly on each coverslip due to error in larval or explant placement. All unique initial distances between competitor positions were adjusted to a common value as described above. However, inter-colony positions at the beginning of the second interval (i.e., at the time of contact) varied among coverslips, rendering comparisons among coverslips after contact meaningless. To correct for this, coordinate data obtained from contact images were transformed in Cartesian space (using basic algebraic and trigonometric functions) such that the orientation of colony positions was identical to the common standardized positions at the beginning of the first interval; i.e., colony positions at the beginning of the second interval were mathematically juxtaposed to be identical to positions at the beginning of the first interval. Since positions of both competitors changed simultaneously during each interval, the start and end positions of each colony were used to determine the relative position change of competitors. This was accomplished by using four distances between competing colony positions from images representing both the start and end of each interval (1 and 2 above): (a) the distance (d1) between competitor positions from the first image, (b) the distance (d2) between the positions of H. symbiolongicarpus from the first image and P. carnea from the second image, (c) the distance (d3) between the positions of P. carnea from the first image and H. symbiolongicarpus from the second image, and (d) the distance (d4) between colony positions from the second image. The following formulas were used to determine the difference between initial and final colony positions relative to one another (Fig. 1):
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Positive values indicated overall position change toward and negative values indicated change away from the "average" position of a competitor. The initial and final distances of each colony relative to its competitor were analyzed among coverslips using paired t tests, with significant deviations from zero indicating position change toward (positive mean) or away from (negative mean) a competitor. In addition to providing information on changes in both direction and magnitude, the paired t test is also robust, having few assumptions of the data (Sokal and Rohlf, 1995).
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Figure 1. Schemata of changes (dashed arrows) in colony position over a single time interval for Podocoryna carnea (pentagons) and Hydractinia symbiolongicarpus (circles) growing on coverslips. The relative change in geometric center of mass (termed "position") of a particular colony from the start (labeled "1") to the end (labeled "2") of each interval was determined by calculating the difference in the distance of that colony from both the start and end positions of its competitors, as shown.
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The outcome of competition was determined when one colony killed and overgrew the other. The number of winning versus the number of losing H. symbiolongicarpus colonies was compared between sexually and clonally produced colonies using likelihood-ratio chi-square.
Larval size
Larvae of each species were generated using the methods described above. The size of larvae was quantified in two ways. First, images of 10 randomly chosen larvae from each of 2 wild-type parental crosses of both species were captured at identical magnification and used to determine the cross sectional area of each using Optimas software. Images were captured when larvae were fully developed and relaxed (about 3 d after fertilization). Larval area was compared between species using a nested analysis with area nested within cross and cross nested within species. Second, 100 larvae from two crosses of H. symbiolongicarpus and 118 larvae from two crosses of P. carnea were each homogenized in 0.5 ml of 0.05% sodium dodecyl sulfate and assayed for total protein using the BCA (bicinchoninic acid) total protein assay with triple-sample replication (Smith et al., 1985). Larvae from the two crosses were pooled to increase the sample size and hence the accuracy of the assay. Because the number of larvae used in the assay differed between species, numbers were standardized prior to comparison.
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Results
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Competition in sexually produced colonies
Of the 30 Podocoryna carnea and Hydractinia symbiolongicarpus primary polyps established on coverslips, 12 P. carnea and 1 H. symbiolongicarpus primary polyp died. This corresponds to a survivorship of 60% of P. carnea and 97% of H. symbiolongicarpus colony initiates.
The relationship of the four response variables (position x and y coordinates of each species) using time as the predictor changed between the time of contact and 14 days post-contact (Fig. 2A; MANOVA, F = 4.96; df = 4, 26; P = 0.0041). Univariate analysis of variance (ANOVA) of each response variable, using time as the predictor, revealed that only the position change of H. symbiolongicarpus colonies along the x-axis was significant (ANOVA, F = 13.54, df = 1, 29, P = 0.0009). There was a near-significant position change of P. carnea colonies along the y-axis (ANOVA, F = 3.40, df = 1, 29, P = 0.0753).
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Figure 2. Colony positions in Cartesian space at each of the three times that images were captured (initiation = symbols with crosses, contact = open symbols, and 14 days post-contact = filled symbols) for sexually produced colonies (A) and clonally produced colonies (B) of Podocoryna carnea (squares) and Hydractinia symbiolongicarpus (circles). The initial distances between competitor positions were adjusted to a common value equal to the average distance between primary polyps or explants among all coverslips. Treated as separate response variables, the remaining data were standardized proportionately to reflect these changes. The x and y coordinates of these data were analyzed for each experiment using MANOVA to detect whether these relationships changed during contact to 14 days post-contact.
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Paired comparisons support the results obtained using MANOVA. Relative inter-colony position did not significantly change prior to contact (interval 1) in colonies of either species (Fig. 3A), although P. carnea position showed a near-significant change away from competitors (for H. symbiolongicarpus: t = 0.84, P = 0.4150; for P. carnea: t = -2.06, P = 0.0556). After contact (interval 2; Fig. 3B), P. carnea position showed a near-significant change away from H. symbiolongicarpus (t = -2.06, P = 0.0603), and there was a highly significant change in H. symbiolongicarpus colony position toward P. carnea after contact (t = 3.88, P = 0.0019).
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Figure 3. The position change (open symbols) of all colonies from a common starting position (filled symbols) of Podocoryna carnea (squares) and Hydractinia symbiolongicarpus (circles) over initial-contact (A, C) and contact–14 d post-contact (B, D) intervals in sexually (A, B) and clonally produced (C, D) colonies. For each colony on a coverslip, the difference between initial and final positions relative to a competitor was analyzed over both intervals using paired t tests, with significant deviations from zero indicating the position change toward or away from a competitor.
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Overall, sexually produced colonies of H. symbiolongicarpus defeated and overgrew their counterparts in 6 of the 17 bouts. Qualitatively, H. symbiolongicarpus winners immediately responded to contact by directional growth of nematocyte-filled hyperplastic stolons toward competitors; these stolons, which often overgrew and destroyed the sparsely arranged stolonal network of P. carnea colonies (Fig. 4), were often produced from existing mat tissue at or near the point of contact. In some cases, H. symbiolongicarpus winners generated defensive dactilozooids. Shortly after contact, many H. symbiolongicarpus winners produced stolonal mat from existing hyperplastic stolons in the region of overlap (Fig. 4C, D). H. symbiolongicarpus losers often grew directionally and produced hyperplastic stolons but were simply unable to overcome their P. carnea counterparts. Likewise, P. carnea winners did not appear to grow differently than losers. Unlike clonally produced colonies in previous studies, sexually produced P. carnea colonies did not produce hyperplastic stolons or dactilozooids upon contact, and they did not display directional growth.
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Figure 4. Image sequence of sexually produced competing colonies. Both species initially adopt a runner-like appearance as primary polyps (A). Hydractinia symbiolongicarpus (at left) begins directional growth toward Podocoryna carnea upon contact (B), after which the former responds by growing nematocyst-filled hyperplastic stolons in the direction of the stimulus. Many H. symbiolongicarpus colonies formed hyperplastic stolons (arrows) that grew directly over and destroyed the foreign tissue (B, C), ultimately forming an ectodermal mat and polyps over the newly acquired space (D). (A) Primary polyps; (B) 2 d post-contact; (C) 7 d post-contact; (D) 14 d post-contact. Scale bars = approx. 2 mm.
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Competition in clonally produced colonies
The relationship of the four response variables (position x and y coordinates of each species) using time as the predictor did not differ between the time of contact and 14 days post-contact (Fig. 2B; F = 2.09; df = 4, 19; P = 0.1218). Univariate ANOVA, using time as the predictor, revealed that only the position change of P. carnea colonies along the x-axis was significant (ANOVA, F = 5.35, df = 1, 22, P = 0.0305).
Relative inter-colony position did not significantly change prior to contact (Fig. 3C) among colonies of either species (paired t tests; t = -1.11, P = 0.2906 for H. symbiolongicarpus and t = -0.38, P = 0.7081 for P. carnea). After contact, P. carnea colony position change was toward H. symbiolongicarpus (Fig. 3D; t = 2.26, P = 0.0474), but there was no significant change in H. symbiolongicarpus colony position relative to P. carnea (t = -1.15, P = 0.2785; Fig. 2).
Overall, P. carnea clonally produced colonies destroyed and overgrew their counterparts in all competitive bouts. A likelihood-ratio chi-square reveals that the outcome of competition was significantly different between clonally and sexually produced colonies (G = 7.9497, P = 0.0048). As previous studies have shown, clonally produced colonies of P. carnea covered available space more quickly than H. symbiolongicarpus, and the former consistently produced hyperplastic stolons upon contact whereas the latter did not. Minimal directional growth was observed in P. carnea after contact, but this growth was qualitatively different from that of H. symbiolongicarpus sexually produced colonies (see Discussion).
Larval size
Larvae differed significantly with respect to cross-sectional area between the species (Fig. 5; nested ANOVA, F = 275.79, df = 1, 2, P = 0.0036). Larvae of H. symbiolongicarpus were 38% larger (average area = 0.062 mm2) than P. carnea larvae (average area = 0.038 mm2). The physical size of H. symbiolongicarpus larvae was consistent with past findings (Weis and Buss, 1987). Because larvae cross-sectional area did not differ significantly between crosses within species (nested ANOVA, F = 0.39, df = 2, 36, P = 0.6772), pooling of larvae generated from the separate parental crosses was validated. The average total protein content was roughly 34% higher in H. symbiolongicarpus larvae (mean value of 6.49 µg/larva) than in P. carnea larvae (4.30 µg/larva).
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Figure 5. Mature planulae larvae of Hydractinia symbiolongicarpus (at left) and Podocoryna carnea. Larvae of the former are significantly larger (nested ANOVA using the cross-within-species effect as the error term, F = 275.79, df = 1, 2, P = 0.0039). Relative larval size was also estimated using the BCA total protein assay. Results revealed that H. symbiolongicarpus larvae contain about 34% more protein on average than P. carnea larvae. Scale bar = approx. 1 mm.
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Discussion
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Previous experimentation using clonally produced colonies has suggested that general life-history patterns of runners and sheets may not apply to these hydroids; that is, the runner-like Podocoryna carnea dominates the sheet-like Hydractinia symbiolongicarpus (McFadden, 1986; Van Winkle et al., 2000). The data presented here support these studies: clonally produced colonies of P. carnea always overwhelmed those of H. symbiolongicarpus. Conversely, sexually produced colonies of H. symbiolongicarpus were able to defeat and overgrow P. carnea in more than 35% of competitive interactions. Hitherto unknown competitive behavior was observed in sexually produced colonies of H. symbiolongicarpus, which showed a highly significant tendency to grow directionally toward P. carnea after contact. Furthermore, most sexually produced H. symbiolongicarpus colonies responded to contact by rapidly generating runner-like hyperplastic stolons from the point of contact that were able to grow directly over P. carnea colonies, which usually lacked hyperplastic stolons during this time. This concentrated projection of hyperplastic stolons progressed until the underlying P. carnea tissue was destroyed, after which the ectoderm between hyperplastic stolons fused to form a mat. In contrast, the clones produced from parental colonies of both species displayed growth patterns similar to those found in previous studies (Tardent and Bührer, 1982; Buss et al., 1984; McFadden et al., 1984; McFadden, 1986; Lange et al., 1992; Van Winkle et al., 2000).
Sexually produced colonies of H. symbiolongicarpus showed morphological as well as physiological features not observed in clonally produced colonies. These differences suggest that growth and development differ qualitatively between the two. First, nearly all sexually produced H. symbiolongicarpus colonies were able to directionally produce hyperplastic stolons, whereas clonally produced colonies did not produce such stolons or grow directionally. Previous studies also report ineffective or little to no hyperplastic stolon production in clonally produced colonies of H. symbiolongicarpus during interspecific bouts (McFadden, 1986; Lange et al., 1992). Unlike P. carnea clones, the capacity of clonally produced H. symbiolongicarpus colonies to generate hyperplastic stolons is highly variable and dependent on colony morphology at the time of contact (McFadden et al., 1984; Buss and Grosberg, 1990; Yund, 1991). In most cases, H. symbiolongicarpus is able to generate hyperplastic stolons only from previously existing stolons (Buss et al., 1984; Lange et al., 1989; Yund, 1991; Grosberg et al., 1996); however, a particular form of underdeveloped mat tissue ("astogenetic" mat) has the capacity to produce hyperplastic stolons (Buss and Grosberg, 1990). In this study, sexually produced colonies of H. symbiolongicarpus initially grew like runners but produced stolonal mat within 2 weeks, thereby giving them their characteristic sheet-like morphology. In contrast, clonal explants of H. symbiolongicarpus produced mat tissue immediately upon attachment to the substratum, as observed in previous studies (McFadden et al., 1984; Blackstone, 1996; Van Winkle et al., 2000). The mat tissue of clonally produced colonies did not develop hyperplastic stolons after contact, suggesting that an astogenetic mat may be an age-specific feature.
Second, H. symbiolongicarpus primary polyps pump gastrovascular fluid to peripheral stolons at a higher rate than those same colonies after mat production, whereas gastrovascular flow rate gradually increases throughout early post-metamorphic development of P. carnea colonies (Blackstone, 1996). Such variation in gastrovascular flow rate may be an important factor mediating colony growth and morphology in hydroids (Dudgeon and Buss, 1996; Van Winkle and Blackstone, 1997; Dudgeon et al., 1999); that is, higher flow rates are associated with more runner-like morphologies. These morphological and physiological differences suggest that sexually produced H. symbiolongicarpus colonies initially adopt a runner-like morphology, which may facilitate their enhanced directional and aggressive growth responses during competition with clonally produced colonies.
To a lesser degree than their counterparts, sexually produced colonies of P. carnea exhibited differences from clonally produced colonies, which more readily and abundantly produced hyperplastic stolons upon contact. The directional growth observed in clonal replicates—and to some extent in sexually produced colonies—most likely represents opportunistic growth into unoccupied areas; that is, clonally produced P. carnea colonies were often able to flank (but not overgrow) their slower-advancing counterparts, which translated into an overall shift in center of mass toward competitors (Fig. 6A). This was not the case in sexually produced H. symbiolongicarpus colonies, which tended to grow hyperplastic stolons from the edge of the ectodermal mat directly into and over the sparsely arranged stolons of P. carnea competitors (Fig. 6B). P. carnea is not able to grow over living H. symbiolongicarpus tissue, presumably due to the space-filling morphology of the stolonal mat. Consequently, H. symbiolongicarpus colonies can survive for extended periods under these circumstances, given that they are able to feed (McFadden, 1986; Buss and Grosberg, 1990; Van Winkle et al., 2000). The ability to generate hyperplastic stolons immediately after contact seems to be an important factor in determining competitive outcome for both species. This was exemplified by the relative success of sexually produced colonies of H. symbiolongicarpus and clonally produced colonies of P. carnea in this study, both of which generated hyperplastic stolons more readily than their corresponding competitors.
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Figure 6. Schemata showing directional growth patterns between clonally produced colonies (A) and sexually produced colonies (B). Podocoryna carnea (gray) clonally produced colonies could not grow directly over their slower advancing Hydractinia symbiolongicarpus (white) competitors and tended to flank them. H. symbiolongicarpus sexually produced colonies tended to project hyperplastic stolons directly over P. carnea colonies soon after contact, whereas clonally produced H. symbiolongicarpus colonies did not.
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Ultimately, the source of every clonally produced colony is a sexually produced colony. Yet critical morphological and physiological aspects of colony development not seen in clonally produced colonies can be observed in very young H. symbiolongicarpus colonies in particular. Sexually produced colonies of H. symbiolongicarpus initially grow like runners, producing both peripheral stolons and presumably astogenetic mat tissue, which suggests age-specific growth that is possible only during a limited time of post-metamorphic colony development. At present, it is impossible to determine the absolute age of the field-collected clones used in this and preceding studies. Thus, the relationship of colony age and competitive ability in H. symbiolongicarpus remains to be quantified using sexually produced colonies. The production of stolonal mat (as opposed to astogenetic stolonal mat) and the deposition of the chitinous understory may divert colony resources from the development and maintenance of morphologies related to competitive ability. Alternatively, a suite of additional factors (e.g., colony size, resource availability, cost of reproduction, somatic maintenance, senescence) may all contribute to the apparent reduction in runner-like growth and competitive ability observed in this species over time (c.f., Braverman and Schrandt, 1966).
The data presented here reveal that during early ontogeny, H. symbiolongicarpus is capable of a pattern of growth and development unprecedented in past studies using clonal replicates. There may be a selective advantage of runner-like growth and enhanced competitive ability during early colony development: in natural populations, the probability of new larval recruitment to gastropod shells decreases with the size and age of resident colonies due to exclusion, and the frequency of competition is thus likewise expected to decrease (Yund et al., 1987; Yund and Parker, 1989). The data presented in this study support the hypothesis that H. symbiolongicarpus is adapted to competition during early colony development. Additionally, the same factors that lead to differential larval settlement over the shell surface (e.g., hermit crab feeding behavior; Yund et al., 1987) are likely to also produce food gradients over the shell surface (c.f., Koehl and Strickler, 1981; LaBarbera, 1984). The directional and runner-like growth potential of young H. symbiolongicarpus colonies leading to the occupation and defense of these nutrient-rich zones may thus provide a significant advantage owing to increased growth rates in early ontogeny. The observed growth and relative success of sexually produced H. symbiolongicarpus colonies may in part explain why this species is considerably more abundant than P. carnea on small gastropod shells inhabited by paguriid hermit crabs. Overall, variation in competitive ability and growth habit between sexually and clonally produced colonies of H. symbiolongicarpus—and to lesser extent between those of P. carnea—suggest that future assessments of competitive ability in colonial organisms (and in colonial hydroids specifically) include the use of sexually produced colonies.
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Acknowledgments
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Comments were provided by R. B. King, J. Miller, B. Johnson-wint, and C. von Ende. Support was provided by the National Science Foundation (IBN-0090580).
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Footnotes
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Received 14 August 2001; accepted 12 December 2001.
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Literature Cited
|
|---|
Bertschy, K. A. 1998. The Influence of Age-specific Survivorship and Growth on Pumpkinseed, Lepomis gibbosus, Life Histories. Canadian Theses Series. National Library of Canada, Ottawa.
Blackstone, N. W. 1996. Gastrovascular flow and colony development in two colonial hydroids. Biol. Bull. 190: 56–68.[Abstract]
Blackstone, N. W., and L. W. Buss. 1991. Shape variation in hydractiniid hydroids. Biol. Bull. 180: 394–405.[Abstract]
Braverman, M. H., and R. G. Schrandt. 1966. Colony development of a polymorphic marine hydroid as a problem in pattern formation. Pp. 169–198 in The Cnidaria and Their Evolution, W. J. Rees, ed. Academic Press, New York.
Buss, L. W. 1990. Competition within and between encrusting colonial invertebrates. Trends Ecol. Evol. 5: 352–356.
Buss, L. W., and N. W. Blackstone. 1991. An experimental exploration of Waddington’s epigenetic landscape. Philos. Trans. R. Soc. Lond. B 332: 49–58.
Buss, L. W., and R. K. Grosberg. 1990. Morphogenetic basis for phenotypic differences in hydroid competitive behaviour. Nature 343: 63–66.
Buss, L. W., and P. O. Yund. 1988. A comparison of recent and historical populations of the colonial hydroid Hydractinia. Ecology 69: 646–654.
Buss, L. W., C. S. McFadden, and D. R. Keene. 1984. Biology of hydractiniid hydroids. 2. Histocompatibility effector system/competitive mechanism mediated by nematocyst discharge. Biol. Bull. 167: 139–158.[Abstract/Free Full Text]
de Kroon, H., and M. J. Hutchings. 1995. Morphological plasticity in clonal plants: the foraging concept reconsidered. J. Ecol. 83: 143–152.
Dudgeon, S. R., and L. W. Buss. 1996. Growing with the flow: on the maintenance and malleability of colony form in the hydroid Hydractinia. Am. Nat. 147: 667–691.
Dudgeon, S., A. Wagner, J. R. Vaisnys, and L. W. Buss. 1999. Dynamics of gastrovascular circulation in the hydrozoan Podocoryne carnea: the one-polyp case. Biol. Bull. 196: 1–17.[Abstract]
Equiza, M., J. Miravé, and J. Tognetti. 2001. Morphological, anatomical and physiological responses related to differential shoot vs. root growth inhibition at low temperature in spring and winter wheat. Ann. Bot. 87: 67–76.[Abstract/Free Full Text]
Frank, S. A. 1993. A model of inducible defense. Evolution 47: 325–327.
Grosberg, R. K., D. R. Levitan, and B. B. Cameron. 1996. Evolutionary genetics of allorecognition in the colonial hydroid Hydractinia symbiolongicarpus. Evolution 50: 2221–2240.[ISI]
Harvell, C. D. 1990. The ecology and evolution of inducible defenses. Q. Rev. Biol. 65: 323–340.[Medline]
Hauenschild, C. 1954. Genetische und entwicklungphysiologische Untersuchungen über Intersexualität und Gewebeverträglichkeit bei Hydractinia echinata Flemm. (Hydroz. Bougainvill.). Wilhelm Roux’ Arch. Entwicklungsmech. Org. 147: 1–41.
Hauenschild, C. 1956. Über die Vererbung einer Gewebeverträglichkeitseigenschaft bei dem Hydroidpolypen Hydractinia echinata. Z. Naturforsch. C 11b: 132–138.
Jackson, J. B. C., L. W. Buss, and R. E. Cook. 1985. Population Biology and Evolution of Clonal Organisms. Yale University Press, New Haven, CT.
Kleijn, D.,J. M. Van Groenendael. 1999. The exploitation of heterogeneity by a clonal plant in habitats with contrasting productivity levels. J. Ecol. 87: 873–885.
Koehl, M. A. R., and J. R. Strickler. 1981. Copepod feeding currents: food capture at low Reynolds number. Limnol. Oceanogr. 26: 1062–1073.
LaBarbera, M. 1984. Feeding currents and particle capture mechanisms in suspension feeding animals. Am. Zool. 24: 71–84.
Lange, R. G., G. Plickert, and W. A. Müller. 1989. Histocompatibility in a lower invertebrate, Hydractinia echinata: analysis of the mechanism of rejection. J. Exp. Zool. 249: 284–292.
Lange, R. G., M. H. Dick, and W. A. Müller. 1992. Specificity and early ontogeny of historecognition in the hydroid Hydractinia. J. Exp. Zool. 262: 307–316.[ISI]
Larwood, G., and B. R. Rosen. 1979. Biology and Systematics of Clonal Organisms. Academic Press, London.
Lundberg, S., P. Nilsson, and T. Fagerstrom. 1996. Seed dormancy and frequency dependent selection due to sib competition: the effect of age specific gene expression. J. Theor. Biol. 183: 1–9.[ISI][Medline]
McFadden, C. S. 1986. Laboratory evidence for a size refuge in competitive interactions between the hydroids Hydractinia echinata (Flemming) and Podocoryne carnea (Sars). Biol. Bull. 171: 161–174.[Abstract/Free Full Text]
McFadden, C. S., M. J. McFarland, and L. W. Buss. 1984. Biology of hydractiniid hydroids. 1. Colony ontogeny in Hydractinia echinata (Flemming). Biol. Bull. 166: 54–67.[Abstract/Free Full Text]
Moora, M., and M. Zobel. 1998. Can arbuscular mycorrhiza change the effect of root competition between conspecific plants of different ages? Can. J. Bot. 76: 613–619.
Muko, S., K. Kawasaki, and K. Sakai. 2000. Morphological plasticity in the coral Porites sillimaniani and its adaptive significance. Bull. Mar. Sci. 66: 225–239.
Müller, W. A., A. Hauch, and G. Plickert. 1987. Morphogenetic factors in hydroids. 1. Stolon tip activation and inhibition. J. Exp. Zool. 243: 111–124.
Plickert, A., A. Heringer, and B. Hiller. 1987. Analysis of spacing in a periodic pattern. Dev. Biol. 120: 399–411.
Smith, P. K., R. I. Krohn, G. T. Hermanson, A. K. Mallia, E. H. Gartner, M. D. Provenzano, E. K. Fujimoto, N. M. Goeke, B. J. Olson, and D. C. Klenk. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150: 76–85.[ISI][Medline]
Sokal, R. R., and F. J. Rohlf. 1995. Biometry, 3rd ed. Freeman, San Francisco.
Spindler, A. N., and W. A. Müller. 1972. Induction of metamorphosis by bacteria and by lithium pulse in the larvae of Hydractinia echinata (Hydrozoa). Wilhelm Roux’ Arch. Entwicklungsmech. Org. 169: 271–280.
Stuefer, J. F. 1996. Potential and limitations of current concepts regarding the response of clonal plants to environmental heterogeneity. Vegetatio 127: 55–71.[ISI]
Tardent, P., and M. Bührer. 1982. Intraspecific incompatibilities in the metagenetical Podocoryne carnea M. Sars (Cnidaria, Hydrozoa). Pp. 295–308 in Embryonic Development, Part B: Cellular Aspects, M. M. Burger and R. Weber, eds. Alan R. Liss, New York.
Umeki, K. 1995. Importance of crown position and morphological plasticity in competitive interactions in a population of Xanthium canadense. Ann. Bot. 75: 259–265.[Abstract/Free Full Text]
Van Winkle, D. H., and N. W. Blackstone. 1997. Video microscopical measures of gastrovascular flow in colonial hydroids. Invertebr. Biol. 116: 6–16.
Van Winkle, D. H., K. Longnecker, and N. W. Blackstone. 2000. The effects of hermit crabs on hydractiniid hydroids. Mar. Ecol. 21: 55–67.
Weis, V. M., and L. W. Buss. 1987. Biology of hydractiniid hydroids. 5. Ultrastructure of metamorphosis in Hydractinia echinata. Postilla 200: 1–24.
Yund, P. O. 1991. Natural selection on hydroid colony morphology by intraspecific competition. Evolution 45: 1564–1573.
Yund, P. O., and H. Parker. 1989. Population structure of the colonial marine hydroid Hydractinia sp. nov. C in the Gulf of Maine. J. Exp. Mar. Biol. 125: 63–82.
Yund, P. O., C. W. Cunningham, and L. W. Buss. 1987. Recruitment and postrecruitment interactions in a colonial hydroid. Ecology 68: 971–982.
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Abstract
Introduction
