Coral Reefs

, Volume 27, Issue 4, pp 783–786

The effect of temperature on larval pre-settlement duration and metamorphosis for the sponge, Rhopaloeides odorabile

Authors

    • School of Marine & Tropical BiologyJames Cook University
  • P. Ettinger-Epstein
    • School of Marine & Tropical BiologyJames Cook University
  • R. de Nys
    • School of Marine & Tropical BiologyJames Cook University
    • AIMS@JCU Tropical AquacultureJames Cook University
Note

DOI: 10.1007/s00338-008-0400-9

Cite this article as:
Whalan, S., Ettinger-Epstein, P. & de Nys, R. Coral Reefs (2008) 27: 783. doi:10.1007/s00338-008-0400-9

Abstract

Rising sea temperatures may potentially affect the dispersive larval phase of sessile marine invertebrates with consequences for the viability of adult populations. This study demonstrated that the planktonic larvae of Rhopaloeides odorabile, a common Great Barrier Reef sponge, survived and metamorphosed when exposed to temperatures up to 9°C above the annual maximum (~29°C). Planktonic larval duration of 54 h, at ambient temperatures (~28°C), were reduced to 18 h for larvae exposed to elevated temperatures (32–36°C). Moreover, at ambient temperatures larvae began metamorphosing after 12 h, but at 32–36°C this reduced to only 2 h. Larvae survived and could still metamorphose at temperatures as high as 38°C, but were no longer functional at 40°C. These results imply that predicted increases in sea surface temperature may reduce planktonic larval duration and dispersal capabilities, thereby contributing to population subdivision of the species.

Keywords

Sessile marine invertebratesLarval settlementThermal-toleranceThermal-stressClimateSponge

Introduction

The mobile larval phase of many sessile marine invertebrates is an important link in determining the biogeography of adult populations (Levin 2006). Mobile larval phases extend adaptive advantages to sessile organisms that include the expansion of species ranges, decreased risks of localised extinction associated with unfavourable habitats or events, and a reduction in the potential for inbreeding (Pechenik 1999). Importantly though, the planktonic larval phase is often a vulnerable stage of the bentho-pelagic lifecycle with high incidences of mortality due to predation, and delivery of recruiting larvae to unfavourable habitats (Rumrill 1990; Pechenik 1999). In addition, environmental parameters including fluctuating sea temperatures also influence larval survival (O’Connor et al. 2007). This raises the question as to whether the effects of rising temperatures associated with changing climate regimes will affect the survivorship, dispersal and recruitment of marine larvae and therefore adult biogeography.

The impact of rapid climate change on both terrestrial and marine ecosystems is topical (Kleypas et al. 1999; Wilkinson 1999; Lough 2007) and there is compelling evidence of the deleterious effect of elevated temperatures on sessile marine invertebrates (e.g., coral bleaching events, Hoegh-Guldberg 1999). Despite embryonic or larval stages having thermal tolerances which are often much narrower than adults (Cossins and Bowler 1987; Przeslawski 2004), some marine invertebrate larvae spend a portion of their life in the upper water column where sea surface temperatures are typically higher (Bassim and Sammarco 2003). Rises in sea temperatures therefore, may not necessarily have the same impact on larval phases for these species. However, higher temperatures can increase the rate of larval development and therefore reduce larval duration with potential consequences for dispersal and population connectivity (O’Connor et al. 2007). Developing an understanding of larval thermal tolerances for marine sessile invertebrates is the first important step in addressing the long-term impacts of elevated temperatures on population dynamics.

This study quantified the effects of elevated temperatures on pre-settlement duration and metamorphosis of larvae from the common Great Barrier Reef sponge Rhopaloeides odorabile. Both pre-settlement duration (time spent swimming) and metamorphosis were tested at a range of environmentally relevant annual temperatures of shallow water reefs (0–12 m) of the Great Barrier Reef where adult R. odorabile commonly occur. Metamorphosis comprised attachment of a larva to the surface of the jar and subsequent invagination, resulting in a flattened disk like form. In addition, the upper thermal tolerance for both pre-settlement duration and metamorphosis were tested because larvae spend time in the upper surface layers (Whalan 2007) where temperatures are likely to be at the higher end of the temperature range.

Materials and methods

R. odorabile is a viviparous dictyoceratid sponge (Demospongiiae), which dribble spawns tufted parenchymella larvae over a period of 5–6 weeks during the Austral summer (Whalan et al. 2007). Larvae were collected from sponges inhabiting the shallow water (9 m) fringing reefs of Pelorus Island, Great Barrier Reef (146°29.58′ E, 18°33.48′S), using larval traps. Ten larvae, <1 h post-release, were placed into each 70 ml sterile plastic specimen jar containing 50 ml of 25 μm filtered seawater (FSW), which were then sealed and suspended in a water bath. Jars (n = 6 per temperature treatment) of larvae were placed into separate water baths at 22, 24, 26, 28, 30, 32, 34, 36, 38 and 40°C and were maintained under conditions approximating a natural photoperiod (12 h light:12 h dark). Jars were monitored at 2 and 6 h, and at 6 h intervals thereafter with the aid of a stereo-dissecting microscope recording metamorphosed, dead or active larvae (i.e. swimming larvae) until all larvae had either metamorphosed or died.

The rapid metamorphosis or death of larvae, at higher temperatures (32–38°C) meant there were no useful comparisons beyond 12 h and was responsible for unequal variances despite arc-sine transformations. Data were therefore analysed in two sections. First, data analysis was undertaken at 12 h using a one-way ANOVA to determine if there was an effect of temperature (22–36°C) on metamorphosis. Second, the data for larvae exposed to temperatures of 22–30°C, met the assumptions of ANOVA and repeated measures ANOVA was used to detect differences for metamorphosis over time. Tukey’s Honest Significant Difference (HSD) post-hoc test was used to detect differences between larval metamorphosis and temperature exposure for both analyses. The effect of temperature (22–36°C) on larval mortality was analysed using the Kruskal–Wallis test on data at 12 h. Analysis was undertaken using SPSS (Version 14.0) software.

Results and discussion

Temperature plays a key role in determining the duration of planktonic larval development and while the effects of temperature on planktonic larval durations have been investigated (modelled) for several sessile marine invertebrates (O’Connor et al. 2007) there are comparatively fewer accounts that quantify the effects of elevated temperatures on larval settlement and metamorphosis. To our knowledge there is a single study that investigates the effects of temperature on sponge larval settlement (Maldonado and Young 1996).

Temperature had a significant effect on R. odorabile larval mortality at temperatures between 22 and 36°C (Fig. 1; K–W test on 12 h data, χ2 = 21.44, df = 7, P < 0.01), but larvae also survived in temperatures up to 38°C for up to 6 h. At the highest temperature of 40°C all larvae died within 30 min. The sealed jars used in this experiment provide a finite air supply, and as a result, depleted air cannot be ruled out as a contributing factor to larval mortality. However, similar mortality levels of larvae with full air exposure at 28–30°C have previously been observed (Whalan 2007) suggesting that other factors contribute to larval mortality. Planktonic larval durations (PLD) were reduced at higher temperatures (32–38°C) to periods as short as 2 h before metamorphosis or death (Figs. 1 and 2). The considerable reduction in PLD at higher range temperatures (32–38°C) in comparison to most lower temperature exposures (22–26 and 30°C) provides support to the theoretical framework proposing elevated temperatures contribute to reduced PLD (O’Connor et al. 2007).
https://static-content.springer.com/image/art%3A10.1007%2Fs00338-008-0400-9/MediaObjects/338_2008_400_Fig1_HTML.gif
Fig. 1

Mean percentage of mortality in Rhopaloeides odorabile larvae for each time period, and at each temperature exposure. Note: For figure clarity error bars have not been included

https://static-content.springer.com/image/art%3A10.1007%2Fs00338-008-0400-9/MediaObjects/338_2008_400_Fig2_HTML.gif
Fig. 2

Mean percentage of metamorphosed Rhopaloeides odorabile larvae over time and at different temperatures. Note: For figure clarity error bars have not been included. Pairwise post-hoc differences (Tukey’s HSD) relate to data at 12 h and as such do not include larval metamorphosis at 38°C which had concluded at 6 h. Significant differences (Tukey’s HSD, P < 0.05) among groups are represented with different letters adjacent to insert legend for temperatures

Although no larvae survived at 40°C, at 38°C larval metamorphosis (or death) had concluded by 6 h suggesting this temperature to be the upper thermal threshold for metamorphosis of R. odorabile larvae, particularly when compared to the levels of larval metamorphosis at 32–36°C (Fig. 2). Metamorphosis at 32–36°C was significantly higher than most lower temperatures (Fig. 2; ANOVA F7,48 = 11.49, P < 0.001). For example, metamorphosis at 32, 34 and 36°C had concluded by 12 h with 52% (±7.72), 60% (±8.8) and 54% (±7.42) metamorphosis respectively. In contrast, metamorphosis at temperatures of 22–26°C was significantly lower [(22°C—2.5% (±1.6); 24°C—18.75% (±7.6); 26°C—20% (±5.98))]. When metamorphosis data were analysed for temperatures between 22 and 30°C, over time, there was a significant interactive effect of temperature and time on metamorphosis (RM ANOVA F10.2,86.9 = 2.15, P < 0.03) with post-hoc tests indicating metamorphosis was significantly different at 28°C in comparison to all other temperatures (22–26 and 30°C).

Determining larval thermal tolerance levels is a key step to developing an understanding of processes that contribute to the biogeography of sessile marine invertebrates. For R. odorabile larvae, temperatures 2–6°C above ambient levels did not inhibit pre-settlement (planktonic) larval durations or metamorphosis, suggesting this species has physiological traits that contribute to its survival in fluctuating temperatures. R. odorabile has clear larval vertical migration behaviours where upon release larvae exhibit an upward migration in the water column (Whalan 2007). This behaviour places them in the upper water column for extended periods before their return to the benthos to settle. As a consequence, this pre-settlement behaviour exposes them to the warmest part of the water column and where they presumably require some degree of thermal tolerance during this key life stage.

While their ability both to survive and metamorphose at temperatures above ambient was clearly demonstrated in the present study the survival and rapid metamorphosis in temperatures up to 38°C was unexpected. Tropical coral reefs experience water temperatures of up to 36°C, although this upper level is only reported in the Persian Gulf (see review Wilkinson 1999). Coral reefs of the Great Barrier Reef experience more moderate sea temperatures with annual regimes generally ranging between 22 and 29°C (Lough 2007). Fluctuations in temperatures beyond this range have significant consequences for a range of sessile coral reef taxa. For example, mean sea surface temperature (SST) in the Great Barrier Reef and other Pacific regions reached 32.7°C during 1998 which resulted in extensive bleaching events of sub-tidal corals (Berkelmans and Oliver 1999) and most likely contributed to bleaching in other benthic invertebrates including clams (Addessi 2001) and sponges (Fromont and Garson 1999). Thermal tolerances of taxa occupying the variable temperature regimes associated with intertidal habitats are presumably higher, however, to our knowledge there is no published information detailing thermal tolerance for benthic marine sessile invertebrate (neritic zone) larvae that compares with the level exhibited by R. odorabile larvae. Indeed, larval thermal tolerances for other dominant tropical benthic invertebrates are comparatively narrower and parallel tolerances closer to adults (Bassim and Sammarco 2003; Negri et al. 2007).

With sea temperatures predicted to rise by 1–3°C over the coming decades on the Great Barrier Reef (Lough 2007) the consequences of larval dispersal on populations is unknown. Based on laboratory manipulations the expected temperature increases may be lethal to some invertebrate larvae (e.g. corals, Bassim and Sammarco 2003). However, for species such as R. odorabile, that can tolerate elevated temperatures, insidious sublethal effects may modify dispersal potential and population connectivity.

It is well established that elevated temperatures contribute to reduced planktonic development periods (O’Connor et al. 2007), however, the scale seen in this study is unprecedented. Therefore, for sessile invertebrates, which rely on planktonic larval dispersal to maintain geographic distributions, reduced larval planktonic durations might interfere with present gene-flow patterns and population connectivity with isolated populations facing an increased risk of localised extinction, particularly if temperatures are above adult thresholds. In common with many brooding sponge species, which have short planktonic periods ranging from hours to days (review Maldonado 2006), R. odorabile have a larval planktonic duration of approximately 2 days (Whalan 2007). The short planktonic period, coupled with poor motilities of sponge larvae (Mariani et al. 2006) often results in restricted dispersal capabilities and subdivided population structures for this group (e.g. Whalan et al. 2005).

Adult R. odorabile occur throughout the central Great Barrier Reef at depths ranging from 5 to 15 m (Wilkinson and Evans 1989). That this sponge occurs in shallow water suggests an ability to deal with conditions associated with shallow water habitats including both fluctuating sea temperatures and high solar radiation. Molecular mechanisms such as the expression of heat shock proteins have been implicated in mediating thermal stress in marine invertebrates including sponges (Efremova et al. 2002), but it is unknown if this capability is also exhibited by larvae. The ability of R. odorabile larvae to survive and metamorphose in both high and low temperatures was a surprising result, but provides a platform for investigations of mechanisms employed by larvae to deal with thermal stress.

Acknowledgements

We thank D. Cocker and A. M. Lynch for assisting in sample collections and laboratory work.

Copyright information

© Springer-Verlag 2008