Mar Biol (2008) 154:833–839 DOI 10.1007/s00227-008-0976-1
ORIGINAL PAPER
Larval settlement and juvenile development of sea anemones that provide habitat for anemoneWsh Anna Scott · Peter L. Harrison
Received: 18 October 2007 / Accepted: 3 April 2008 / Published online: 15 April 2008 © Springer-Verlag 2008
Abstract Sea anemones that host obligate symbiotic anemoneWsh are ecologically important throughout many coral reef regions of the Indo-PaciWc. This study provides the Wrst quantitative data on larval settlement rates and juvenile development of two species of host sea anemone, Heteractis crispa and Entacmaea quadricolor. Larvae were reared from broadcast spawned gametes of sexually reproductive male and female anemones collected from the Solitary Islands Marine Park, NSW, Australia. Prior to the start of the experiments, H. crispa larvae were reared for 3 days after spawning in March 2004 and E. quadricolor larvae were reared for 4 days after spawning in February 2005. Larval settlement onto biologically conditioned terracotta tiles in outdoor Xow-through seawater aquaria was Wrst recorded 4 days after spawning for H. crispa and 5 days after spawning for E. quadricolor. Peak settlement occurred 10 days after spawning, with a mean of 33.4 and 50.3% of the original groups of 350 larvae in replicate tanks settling for H. crispa and E. quadricolor, respectively. Tentacles arose as outpocketings of the oral region, at Wrst appearing as small rounded buds. These buds elongated to form long, thin, tapering tentacles in H. crispa,
Communicated by J.P. Grassle. A. Scott (&) National Marine Science Centre, PO Box J321, CoVs Harbour, NSW 2450, Australia e-mail:
[email protected] A. Scott · P. L. Harrison Coral Reef Research Centre, School of Environmental Science and Management, Southern Cross University, PO Box 157, Lismore, NSW 2480, Australia e-mail:
[email protected]
whereas E. quadricolor tentacles had slight bulbs below the tips. Juvenile anemones, especially H. crispa, were found to have very diVerent colouration and markings when compared with adult anemones, and therefore the descriptions and images provided here will enable correct identiWcation of juvenile recruits.
Introduction Larval settlement in cnidarians occurs when the planula ceases to swim or crawl, attaches to the substratum and then undergoes metamorphosis into a juvenile polyp (Campbell 1974; Leitz 1997; Harrison and Booth 2007). Settlement is generally preceded by intensive larval searching and testing of the substratum, suggesting microhabitat selection (Fadlallah 1983; Harrison and Wallace 1990). The potential for active substratum selection has obvious advantages in enhancing post-metamorphic survival and there is now considerable evidence that settlement is not a random process (Chia and Bickell 1978; Fautin et al. 1989; Martin and Koss 2002). In some species, especially those with brooded larvae, settlement may be achieved within a few hours; however, for most broadcast spawning species the larvae may remain within the water column for days, weeks or sometimes months before they settle (Richmond 1987; Harrison and Wallace 1990; Nozawa and Harrison 2002; Harrison 2006). Metamorphosis occurs when the larvae undergo morphological and physiological changes that are largely irreversible (Negri et al. 2001) and by deWnition, comprises the loss or transformation of larval structures and the elaboration of adult structures (Müller and Leitz 2002). Partial metamorphosis of anthozoan larvae often begins prior to settlement, having undergone the morphogenetic processes
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that produce the mesenteries, mouth, actinopharynx and musculature (Stephenson 1928; Widersten 1968; Fautin et al. 1989). The Wnal stages of metamorphosis, which result in the formation of a juvenile polyp typically take place after attachment to the substratum (Riemann-Zürneck 1976). Previous studies on larval settlement of broadcastspawning or brooding sea anemones have sometimes had problems with achieving settlement and metamorphosis of the planulae (Gemmill 1921; Chia et al. 1989; Weis et al. 2002; Davy and Turner 2003). This most likely indicates sub-optimal settlement conditions such as inappropriate settlement substrata or lack of important metamorphosis cues (Harrison and Wallace 1990; Miller and Mundy 2003). Currently, there is no published scientiWc information on larval settlement and metamorphosis of any of the ten species of sea anemone that are known to provide essential habitat for 28 species of obligate symbiotic anemoneWsh. Symbioses between the anemoneWsh and their host anemones typically occur on or near coral reefs, in the shallow sunlit waters of the tropical and suitable subtropical parts of the Indo-PaciWc (Mariscal 1970; Dunn 1981; Fautin and Allen 1992). The present study documents the settlement rates and juvenile development of two host sea anemone species, Heteractis crispa and Entacmaea quadricolor, providing important insights into the early life stages of these species and increasing the understanding of the processes that maintain and renew host sea anemone populations.
Methods and materials Experimental set up Thirty to forty anemones, H. crispa and E. quadricolor, were collected from rocky reefs at 9–18 m depth in the Solitary Islands Marine Park, NSW, Australia (29º55⬘S, 153º23⬘E), and maintained and monitored in outdoor Xowthrough seawater tanks at the National Marine Science Centre, CoVs Harbour for spawning activity (Scott and Harrison 2007a). Male and female anemones broadcast spawned their gametes during a few nights of each year in late austral summer and autumn after the full moon (Scott and Harrison 2007a). For each species, the spawned gametes were collected and gently mixed to promote genetic diversity. The resulting embryos and larvae were reared in 60-l plastic tubs containing seawater and gentle aeration (Scott and Harrison 2007a, b). Larval settlement experiments were set up 3 days after H. crispa spawned on the 9 March 2004 and 4 days after E. quadricolor spawned on the 25 February 2005 (Scott and Harrison 2005, 2007a). Five groups of 350 H. crispa larvae and four groups of 350 E. quadricolor larvae were counted
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using a tally counter and a Bogorov plankton tray viewed under a dissecting microscope and illuminated with a Wbre– optic light source. Once counted, the larvae were placed into replicate 33-l aquaria. Each aquarium contained a settlement cage with four 250 m mesh panels in the sides and a terracotta settlement tile (11 £ 11 £ 1 cm) that had been biologically conditioned at North Solitary Island for approximately 1 month prior to the start of the experiments (after Harrison 2006). Tiles were placed horizontally approximately 1 cm above the bottom of the settlement cage using plastic frames at opposite tile corners. The upper surface of the tile was approximately 7.5 cm below the water surface. The aquaria were supplied with Xow-through Wltered (30 m) seawater at a rate of approximately 0.6 l min¡1 to maintain ambient water quality and were located outdoors to provide natural lighting and photoperiod. Mean monthly seawater temperature ranged from 19 to 25°C throughout the study period. Larvae and juveniles were potentially able to feed on dissolved nutrients and particulate matter in the Xow-through seawater, and receive photosynthate translocated by symbiotic zooxanthellae. Nutrition was supplemented by Aquasonic liquid invertebrate food. Monitoring of settlement Settlement of H. crispa and E. quadricolor larvae and their subsequent development into juvenile anemones was monitored at set intervals from 4 to 94 days after spawning. Each settlement tile was transferred into a shallow tray of seawater and observed using a monitoring grid and a Leica S6D dissecting microscope illuminated with a Wbre–optic light source. The number of individuals occurring on the upper and lower surfaces and edges of the tiles, and the interior of the settlement cages was counted, with the stage of development for each individual being recorded. As recently attached larvae have the ability to resume swimming and metamorphosed juveniles remain mobile even after settlement, the numbers recorded represent the individuals present at each sampling time. This is the outcome of previously and newly settled individuals less any mortality or movement oV the tiles that may have occurred between sampling times. Once monitoring was completed the tiles were returned to the aquaria until the next census. Excessive algal growth became apparent on some of the H. crispa settlement tiles 157 days after spawning and began to smother the juveniles. At this point, the juveniles were gently removed and combined into two replicates with biologically conditioned settlement tiles that had a lower algal biomass. Monitoring of these tiles continued in the same manner as described above until one year after spawning; however, these data were used only for monitoring juvenile development.
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Data analysis A multilevel regression model was used to test if the total settlement rates of H. crispa and E. quadricolor larvae diVered from one another at the various sample times. Multilevel regression models are very useful for analysing hierarchical data structures that include nesting within groups and repeated measures designs (Singer 1998; Snijders and Bosker 1999; Hox 2002). The model was Wtted via Restricted Maximum Likelihood using the MIXED procedure in SPSS, version 14.0. The model chosen to determine if total settlement rates diVered between species included sampling time (at 12 levels), species (at two levels), and the monitoring by species interaction as the Wxed factors. The Wxed factor results are presented in an ANOVA type format in this paper, while the parameter estimates can be found in Scott (2007). The random factors of the model included tank and time to account for the longitudinal nature of the data. Walds Z test was used to test the signiWcance of the variance components of the model. At each sampling time, pairwise comparisons were made between species for total settlement. Bonferroni correction was used to adjust for multiple comparisons.
Results Settlement over time The multilevel regression model showed that the eVect of sampling time was signiWcant, while the eVect of species was not (Table 1). The sampling time by species interaction was also signiWcant, which indicates that the total number of settled individuals varied with time. The parameter estimates for the random eVects of the model indicate that there was no signiWcant variance from zero at any of the sampling times or in terms of tank variance (Table 2). Settled H. crispa and E. quadricolor individuals were found during the Wrst sampling time, i.e. the day after the experiments were set up (Fig. 1). Peak settlement occurred 10 days after spawning for both species, with total mean settlement of 116.6 (SE § 12.2) individuals for H. crispa
Table 1 Type 1 tests of Wxed eVects for the multilevel regression model for diVerences in total settlement between H. crispa and E. quadricolor over time Factor
Denominator df
F
P
Sampling time
9.927
6.967
0.002**
Species
9.815
0.014
0.909--
Sampling time £ species
9.620
8.397
0.001***
*** P · 0.001, **P · 0.01, *P · 0.05, --P > 0.05
Table 2 Parameter estimates and corresponding standard errors for the random eVects of the multilevel regression model for diVerences in total settlement between H. crispa and E. quadricolor over time Parameter
Variation over time
Sampling time
Estimate
SE
Walds Z
P
1
2724.08
1466.39
1.858
0.063--
2
3150.59
1696.46
1.857
0.063--
3
3284.68
1768.45
1.857
0.063--
4
1981.87
1071.77
1.849
0.064--
5
773.31
423.84
1.825
0.068--
6
36.35
31.75
1.145
0.252--
7
114.49
78.32
1.462
0.144--
8
70.13
50.91
1.378
0.168--
9
70.44
50.23
1.402
0.161--
10
37.16
32.17
1.155
0.248--
11
264.30
163.69
1.615
0.106--
12
121.93
79.62
1.531
0.126--
463.37
254.56
1.820
0.069--
Tank variance
*** P · 0.001, **P · 0.01, *P · 0.05, --P > 0.05
and 176.0 (SE § 40.9) individuals for E. quadricolor. While the mean number of settled E. quadricolor individuals was higher in comparison to H. crispa, the Bonferroni adjusted pairwise comparison was not signiWcant due to high between tank variation (Fig. 1). After the peak settlement period, the mean number of E. quadricolor juveniles decreased sharply until 38 days after spawning, and then declined gradually to 21.0 (SE § 7.6) by the end of the experiment. In contrast, the number of settled H. crispa juveniles remained fairly stable over time, with a mean of 77.0 (SE § 12.2) at the end of the experiment. From day 52 onwards, the mean number of H. crispa juveniles was signiWcantly greater than the mean number of E. quadricolor (Fig. 1). Development and growth of juvenile anemones Initial attachment Prior to attaching, H. crispa and E. quadricolor larvae were observed to slowly creep or rotate along the surface of the substrata, stopping momentarily before swimming oV again. Larvae attached to the substrata by their aboral pole. This initial attachment was easily disturbed; however, it became stronger with time. Attached H. crispa and E. quadricolor individuals were elongate or pear shaped with an oral pore and zooxanthellae inherited from the maternal parent scattered throughout their endoderm. Once attached, the column shortened, the larva became squat, and a mouth and small tentacle buds appeared. These buds later elongated to form tentacles. Settled juveniles of both species were occasionally observed to glide across the substratum,
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Attached H. crispa individuals were generally dark green to brown (Fig. 2a), changing to cream to brown with time. Tentacles arose as outpocketings of the oral region, at Wrst appearing as small rounded buds before elongating to form long, thin, tapering tentacles (Fig. 2b, c). A small mouth was visible at this stage. The majority of individuals had eight tentacles 6 days after spawning. These tentacles were
evenly spaced around the oral disc and generally of equal length; as subsequent tentacles were added, usually in multiples of two, the length of the tentacles varied (Fig. 2d). The oral disc developed a speckled white and brown appearance 10 days after spawning, and the mesenterial insertions were visible as slight furrows on the otherwise Xat and broad surface (Fig. 2d). The mouth was well developed and feeding was Wrst observed 17 days after spawning. Mesenterial insertions formed longitudinal bands on the column, and white banding on the tentacles became apparent 17–24 days after spawning. The white bands sometimes created ridges on the tentacles, leading to slight bulbs. A circle of white dots around the outside of the oral disc was also present in some individuals. Juvenile anemones with up to 20 tentacles were present 92 days after spawning. Purple colouration developed on the tips of the tentacles 157 days after spawning, and 196 days after spawning the tentacles had a slight green tinge. The oral disc of most individuals was speckled white and brown, with a white ring around the periphery. Some individuals started to develop a greenish colouration in their oral disc 247 days after spawning. A second circle of tentacles was formed inside those bordering the oral disc 287 days after spawning. During the early stages of growth and development, the circular pedal disc of the settled juveniles was approximately the same size as the oral disc and column. As development proceeded the oral disc increased in diameter. As a result the column tapered from the oral disc to the pedal disc. Small verrucae were visible in longitudinal rows on the column, becoming numerous and prominent by the time the juveniles were one-year-old (Fig. 2e). At this stage the
Fig. 2 Settlement, metamorphosis and juvenile development of H. crispa: a elongate planula loosely attached to the substratum (4 days after spawning); b juvenile starting to develop small tentacle buds (6 days after spawning); c eight small tentacle buds (10 days after spawning); d eight tentacles plus two small tentacle buds, white pig-
mentation on oral disc and single bands on some tentacles (24 days after spawning); e 12-month-old juvenile, second circle of tentacles apparent, multiple white bands on most tentacles and white ring around oral disc; f 13-month-juvenile, verrucae and longitudinal banding on column, purple colouration on tips. Photographs A. Scott
Fig. 1 Settlement patterns of H. crispa and E. quadricolor larvae, including all tile surfaces (upper, lower, edges) and cage. Mean settlement is represented by solid lines and circles (§SE). Mean percentage settlement is represented by dotted lines and triangles. H. crispa is represented by black and E. quadricolor by white. ***P · 0.001, **P · 0.01, *P · 0.05 indicate the signiWcance level of the Bonferroni adjusted pairwise comparisons
so that the initial point of attachment was not necessarily the site where the juvenile remained. Morphological development of H. crispa
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juvenile anemones had approximately 60 tentacles and long striations running the length of the column in groups of four (Fig. 2f). Morphological development of E. quadricolor Newly settled E. quadricolor anemones were brown to orange (Fig. 3a, b). The column became more orange than brown over time and zooxanthellae densities increased; accumulating mainly in the tentacles and oral disc (Fig. 3c, d). The majority of individuals had 12 tentacles that were of varying length and arranged in a particular order by the time they were 7 days old (Fig. 3d). Individuals started to develop white pigmentation and slight bulbs in their tentacles 10 days after spawning (Fig. 3e). Generally, three of the 12 tentacles were longest, the next three were slightly shorter, and the remaining six were shorter again (Fig. 3f). The three longest tentacles were usually frosted white and held higher than the other tentacles, having a bulb just below the tip. This bulb was also usually present in the three slightly shorter tentacles. The remaining six tentacles lacked bulbs and were generally orange to pink. When expanded, the tentacles, oral disc and column were translucent and the mesenteries were visible through the oral disc as longitudinal lines on the column. Each tentacle arose from an intermesenteric space and the mesenterial insertions caused small indentations in the oral disc and column. The pedal disc was usually about the same width as the column, which was smooth and of approximately equal width throughout its length. Retractor muscles were visible through the oral disc and what appeared to be nematosomes, i.e. small clusters of cells that bear nematocysts and move around without permanent attachment to the body of the anemone (Crowell 1946), could sometimes be seen through the oral disc, tentacles and column.
837
The mouth was elongate and slightly darker than the oral disc, the lips were usually bright pink and white spots were sometimes present at the directive ends of the mouth (Fig. 3f). The tentacles became dark brown 52 days after spawning. The purple column, which is characteristic of many adult anemones found at North Solitary Island, started to develop 94 days after spawning. The maximum number of tentacles observed during the experiment was 16.
Discussion Settlement and metamorphosis of planulae into primary polyps are crucial phases in the life history of broadcast spawning cnidarians, such as H. crispa and E. quadricolor. The larvae of both species readily settled on a variety of surfaces including the biologically conditioned terracotta settlement tiles, the bottom and sides of the plastic settlement cages, and the mesh panels of these cages. In contrast, the planulae of other anemones such as Aiptasia tagetes (see Riggs 1988), Anthopleura ballii (see Davy and Turner 2003), Anthopleura elegantissima (see Siebert 1974; Weis et al. 2002), Gonactinia prolifera (see Chia et al. 1989), and Haliplanella lineata (see Fukui 1991) have not been observed to undergo successful settlement and metamorphosis in the laboratory. In some cases these larvae were oVered a variety of substrata and inducers. SpeciWc cues inducing settlement and metamorphosis may emanate from the substrata (Morse et al. 1988; Leitz 1997; Heyward and Negri 1999; Negri et al. 2001). Given that H. crispa and E. quadricolor larvae displayed searching behaviour prior to settlement it is probable that they were testing the substrate for metamorphic cues. Most solid surfaces in the marine environment are rapidly colonised by bacteria, some of which are known to induce larval settle-
Fig. 3 Settlement, metamorphosis and juvenile development of E. quadricolor: a elongate planula attached to substratum (5 days after spawning); b juvenile starting to develop small tentacle buds (5 days after spawning); c small tentacle buds (5 days after spawning); d 12 tentacles (7 days after spawning); e 12 tentacles, starting to develop bulbs, white pigmentation on tentacles and around oral disc (10 days after spawning); f 12 tentacles, six longest with bulbs and the longest three being white (17 days after spawning). Photographs A. Scott
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ment (Müller and Leitz 2002). Bacteria are likely to have colonised the surfaces within the settlement cage, possibly rendering them suitable for H. crispa and E. quadricolor larval settlement. Although settlement of H. crispa and E. quadricolor larvae was recorded the day after the experiments were set up (4 and 5 days after spawning, respectively) this does not necessarily indicate the age at which larvae were Wrst competent to settle, as some E. quadricolor larvae were found to have settled in the larval rearing containers 3 days after spawning (A. Scott personal observation). The timing of settlement in these species was still much shorter than has been previously reported for other broadcast spawning sea anemones such as Nematostella vectensis, which settled 7 days after spawning in similar water temperatures (Hand and Uhlinger 1992). The majority of H. crispa and E. quadricolor larvae settled within 10 days after spawning, which is similar to many species of reef coral larvae (Harrison et al. 1984; Babcock and Heyward 1986; Harrison 2006). Likewise, the peak settlement rates recorded for H. crispa and E. quadricolor were similar to those found for the broadcast spawning coral Favites chinensis (Nozawa and Harrison 2005). After settlement reached a peak, the number of settled H. crispa and E. quadricolor juveniles decreased with time, with the latter having higher rates of mortality. Heteractis crispa and E. quadricolor juveniles were able to change position after metamorphosis had taken place. With increasing age mobility decreased and attachment to the substratum became stronger. The ability to change position on the substratum after settlement is a trait shared by other anemones. For example, juvenile Anthopleura xanthogrammica are much more mobile than the adults (Sebens 1981). This diVers from some other cnidarians such as scleractinian corals where metamorphosis transforms the motile planula into a sessile polyp (Chia and Bickell 1978; Harrison and Wallace 1990; Richmond 1997). Post-settlement juvenile mobility may allow anemones to space themselves away from the tentacle crowns of other individuals, thus reducing competition for prey. Furthermore, although larvae have the ability to select juvenile habitat, mobility may provide the opportunity for secondary habitat selection, allowing more appropriate adult habitat to be selected at a later stage of development (Sebens 1981). The white oral disc and markings on the tentacles of juvenile H. crispa anemones are not characteristic of the adults found at North Solitary Island. On 12 February 2005, a juvenile anemone of this species was observed during a collecting dive at the Canyons on the western side of the island (C. Damiano and A. Scott personal observation). This individual displayed the same markings and colouration as the juvenile anemones bred and reared in experimental aquaria. This indicates that colouration varies
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greatly between juvenile and adult stages, and that successful sexual reproduction and recruitment of this species occurs in the Weld at the study location. As juvenile anemones, particularly H. crispa, were found to have very diVerent colouration and markings when compared with adult anemones, the descriptions and images provided here will enable correct identiWcation of these species during studies of recruitment, a subject that is poorly understood. Acknowledgments We thank Margaret Rolfe and Lyndon Brooks who provided substantial statistical advice and support with data analyses. This paper forms part of a Ph.D. thesis submitted by A. Scott to Southern Cross University, Lismore. This research was funded by the Australian Geographic Society, Project AWARE Asia PaciWc, NSW Marine Parks Authority, and SCU Postgraduate grants. Research was conducted in accordance with the conditions speciWed by NSW Fisheries Permit P02/0025 and complied with the current laws of Australia.
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