Records of the Western Australian Museum Supplement No. 69: 11-21 (2006).

'The population dynamics and feeding preferences of Bursatella leachii (Opisthobranchia: Anaspidea) in northeast Queensland, Australia

Cathryn L. Clarke James Cook University, Townsville, Queensland 4811, Australia Email: [email protected]

Abstract - Sea hares (Opisthobranchia: Anaspidea) have long been known to form dense aggregations in shallow marine habitats. However, there have been few attempts to document the dynamics and causes of these aggregations. The present report investigates the population dynamics of Bursatella leachii found in association with a cyanobacterial bloom in tropical north Queensland, Australia. The aggregation was fuelled by a continual source of recruits and in laboratory testing, this population preferred a green alga to its prey item in the field, the cyanobacterium, Calothrix crustacea. Therefore, B. leachii has the ability to continually recruit in large numbers to seagrass beds in order to exploit an abundant but less preferred food resource. Key words: Bursatella leachii, 5tylocheilus striatus, sea hare, Anaspidea, feeding preference

INTRODUCTION preference for low-intensity wave action and their The single unifying feature of all populations is preference for intertidal algae species. In one year, their dynamism. Documenting natural population Plaut et al. (1998) observed a rare algal bloom in fluctuation has become increasingly important in deeper water and Aplysia oculifera was found in recent times where the need exists to distinguish greater abundance in association with this bloom natural fluctuations in systems from those caused than those populations in the exposed shallow­ by anthropogenic disturbance. The majority of water habitats. fluctuations in populations occur on a local scale The second hypothesis is that the sea hares settle (Smith 1996). Aggregations of large numbers of in a range of habitats and migrate to areas of highly animals in a single area are an extreme example of dense conspecifics for the purpose of breeding. In population fluctuation. These events are referred to California surf-grass beds, Aplysia californica form as population explosions or irruptions (Colgan dense breeding aggregations in summer months 1987; Burla and Ribi 1998; Cote and Reynolds 1998; (Audeskirk 1979). Breeding aggregations of B. Williams et al. 2001). These aggregations are often leachii during the Florida winter were also observed an obvious and highly visible incident to human but animals in summer aggregations were mostly visitors to the site in question and can have a strong immature (Lowe and Turner 1976). effect on the local animal and macrophyte The third hypothesis for aggregation is that it communities. occurs where food is localized (Carefoot 1987). In A range of largely anecdotal evidence suggests habitats where food is concentrated sea hares may that some sea hare species exhibit boom-and-bust aggregate incidentally as a result of larval cycles, forming large aggregations and then settlement or feeding preferences. That is, a large disappearing. There are a number of hypotheses as recruitment of sea hares may settle in an area where to why populations of sea hares exhibit this a preferred host alga is high in abundance. In Israel, dynamic. One hypothesis for the cause of A. oculifera abundance was highly correlated with aggregation is a response to hydrological the variable presence of species of Ulva and conditions. Lowe and Turner (1976) hypothesized Enteromorpha (Plaut et al. 1998). A. californica that aggregations of juvenile Bursatella leachii were juveniles for example, are primarily found on the caused by the hydrological conditions in subtidal red algae Plocamium cartilagineum and Laurencia habitats. In addition, the intensity of water pacifica (Pennings 1991). However, Pawlik (1989) movement in Israel intertidal habitats was demonstrated that A. californica settles on a wide negatively related to adult sea hare abundance range of algae and crawls to the preferred species. (Plaut et al. 1998). The occurrence of sea hares in Sites with greater P. cartilageum cover contained intertidal habitats may be a compromise between a higher numbers of A. californica recruits however 12 c.L. Clarke this characteristic did not explain the variation in negatively correlated with macrophyte toughness recruitment intensity which may be related to larval and calcification in D. auricularia. In addition, the supply (Pennings 1991). The combination of feeding preferences of A. californica have been found favourable larval conditions and a high abundance to expand with ontogenetic development (Pennings of a preferred algae species for competent larvae 1990b) and this trend was thought to be caused by may cause high settlement of juveniles in these the soft, weak mouth parts found in younger areas. individuals. The key to this last hypothesis is the feeding Biotic interactions, either competition or preference of the sea hare species under predation, have also rarely been examined as investigation. On the whole, feeding specialists influences on feeding preferences in sea hares. seem to be relatively rare in the marine Competition has been suggested by some authors environment when compared with terrestrial (Willan 1979; Achituv and Susswein 1985) although systems (Lubchenco and Gaines 1981; Hay et al. never directly tested. Two studies on the influence 1989). In contrast, most sea hares are relatively of predation on feeding preferences yielded specialized feeders and there is a substantial body contradictory results (Pennings 1990a; Rogers et al. of work addressing the feeding preferences of 2000,2002). various species (Carefoot 1967, 1987; Wu 1980; Stylocheilus striatus and B. leachii are often Pennings 1990b; Pennings et al. 1993; Rogers et al. reported to be found in dense feeding aggregations 1995; Nagle et al. 1998). These studies had mixed in association with blooms of cyanobacteria results and it can be difficult to sort out the factors (Switzer-Dunlap and Hadfield 1979; Paul and influencing feeding preference in sea hares. Factors Pennings 1991). The dynamics of these aggregations such as nutritional value, abundance, secondary has never been quantitatively examined for either chemistry and biotic interactions have previously of these two species. A sole report, Lowe and been the focus of sea hare feeding preference Turner (1976) examined aggregations of B. leachii at studies. Analyses of the nutritional qualities of a beach in Florida but measured the densities of algae tested for sea hare feeding preferences have animals washed up on the shoreline, therefore largely failed to correlate specific qualities with giving no indication of the natural density of this feeding preferences (e.g., Carefoot 1967, 1970; species. The temporal dynamics of these types of Rogers et al. 1995). aggregations have not been previously investigated Foraging theory states that feeding on the most and therefore, the underlying cause of population abundant and therefore readily obtainable food irruption in sea hares is unknown. In addition, the sources will require the least energy and thus is feeding preferences of B. leachii have not been most advantageous to the herbivore (Crawley determined for tropical populations. This report 1983). We would expect therefore that sea hares tests the third hypothesis as the cause for the would prefer abundant algae. This is true for some aggregations observed in tropical North species under certain conditions. For example, the Queensland; that is, aggregations caused by specialist sea hare, Aplysia juliana, feeds on and common feeding preferences. The population occupies the abundant green alga, Ulva lactuca, both dynamics of this aggregation were examined using in the laboratory and in the field (Carefoot 1970; descriptive length-frequency analysis to test Rogers et al. 1995). In contrast, Aplysia parvula whether B. leachii settled in a single pulse of utilizes two species of algae which are rare in the recruitment. Laboratory feeding preference was local environment (Rogers et al. 1995). tested to shed light on whether these sea hares were Numerous studies have examined the influence aggregating in response to a preferred food item. of algal secondary chemistry on the feeding preferences of sea hares. Investigations into the role of these chemicals have produced mixed results. MATERIALS AND METHODS The generalist herbivore, Dolabella auricularia, was relatively unaffected by the presence of chemical Population monitoring defences in the host algae (Pennings and Paul 1992). Sea hare population sampling was conducted at a Yet, other sea hare species seem to be substantially site in Cleveland Bay near Townsville, Queensland, affected by the type and concentration of Australia (19°10'S, 146°45'E). Cleveland Bay is a macrophyte secondary metabolites (Stylocheilus shallow embayment spanning 30 km protected striatus: Nagle et al. 1998; A. parvula: Ginsburg and from the prevailing winds by Magnetic Island, Cape Paul 2001). Cleveland and the Great Barrier Reef (Lanyon and Physical characteristics of the host macrophyte Marsh 1995). Cleveland Bay is slightly turbid as a have been mostly overlooked in general studies on result of freshwater runoff from local creeks, a sea hare feeding preferences. One exception is the shipping channel and re-suspended sediment from study by Pennings and Paul (1992) where the wave turbulence (Walker and O'Donnell1981). The authors demonstrated that low preference is tidal pattern in these waters is mixed semi-diurnal. Population dynamics and feeding preferences of Bursatella leachii 13

Cleveland Bay is tropical but experiences large aquaculture facility. Sargassum sp. (Phaeophyta: seasonal variation in rainfall and minor Fucules) and P. pinnata (Rhodophyta) were chosen temperature changes between summer and winter for their abundance in areas where B. leachii is months (Lanyon and Marsh 1995). found along the coast of Queensland, although they The study site, Shelly Beach, is a shallow bay were not abundant at the site where the animals covered by seagrass beds dominated by three were collected. Red and brown algae were only species, Halodule uninervis, Halophila ovalis, and present at extremely low densities in the study site Zostera capricornis. The site is located at the northern so Sargassum sp. and P. pinnata were collected from end of Rowes Bay and faces east towards Magnetic Kissing Point, Rowes Bay, Townsville. Island. Mangrove forest lies at the northern end and For feeding preference assays, 40 individual B. a rocky point at the south end. Shelly Beach is an leachii were collected at low tide from the study site. ideal place to closely examine the population Animals were placed in fresh seawater in 1L dynamics of S. striatus and B. leachii because of the containers and transported back to the laboratory relative simplicity of the benthic habitat. The Shelly located in the Marine Biology and Aquaculture Beach seagrass beds are never completely dry Research Facility Unit (MARFU) aquarium system because some water is retained even at extremely at James Cook University (JCU). All B. leachii were low tides. Therefore sampling can be completed at placed in a large aquarium (maintenance tank) low tide as sea hares are not forced to migrate by supplied with continuously flowing filtered dropping water levels. seawater (salinity -33ppt, pH - 8.0, temperature Five sampling trips were made to the Shelly 27-28°C). Animals were held overnight to allow Beach seagrass beds on 25 June, 7 July, 21 July, 27 acclimatisation before experimentation. Both July, and 3 September 2002. On each trip three 25 x maintenance and experimental tanks were on a O.5m belt transects were run parallel to the beach, 12h:12h light:dark diel cycle. 2 yielding an estimate of sea hare density per 125m . Transects were run at approximately lOOm from the Feeding assays shore and were always oriented parallel to the Sixteen replicate 1.5L aquaria supplied with beach to eliminate the effect of tidal height and to continuously flowing filtered seawater acted as the keep the measurement area within the dense experimental arenas. Pre-weighed, equal amounts seagrass habitat. Within each transect the sea hare (approximately 2 g wet weight) of each of two species present and the number and length of species of macroalgae or cyanobacteria were placed individual sea hares was recorded. The sea hare at opposite ends of each experimental arena. For species present was identified according to each two-way choice experiment, eight Coleman (2001). The length of each sea hare was measured by placing the individual on the transect experimental tanks and eight control (no-herbivore) tape and allowing the animal a few seconds to start replicates were used. Control tanks were identical to crawl along it. Once crawling, the distance in design and set-up, except for the absence of the between the base of the cephalic tentacles and the herbivore. The loss of algae in the control tanks was tip of the tail was recorded. The number of sea hare used to calculate the loss of algae due to autogenic egg masses observed within transects was also change from natural breakdown in the recorded, although the species of egg mass could experimental tanks. Experimental tanks were not be identified in the field. randomly assigned at the start of each trial to During the five sampling trips, algae for remove the possibility of any single aquaria­ laboratory feeding preference testing were associated bias. At the commencement of a trial, the collected. In total, three species of macroalgae wet weight of each alga in each tank was recorded (Enteromorpha 1 sp., Sargassum sp., and Pterocladia and a randomly chosen B. leachii from the pinnata) and one species of cyanobacterium maintenance tank was placed at the centre of each (Calothrix crustacea) were tested. The latter species experimental tank. Individual sea hares were was the cyanobacterium found in the cyanobacterial allowed to move about the experimental tank and bloom where the sea hares were collected and was feed for a 24-hour period. Five times over the an observed prey item of B. leachii in the field. course of the trial, the position of each individual Filamentous C. crustacea was collected directly from sea hare was recorded and scored as to presence on seagrass beds at Shelly Beach, growing alga I, alga 2, or on the tank walls (Attractiveness epiphytically on seagrass blades or the benthos. The trial). At the termination of the trial, all algae was green alga, Enteromorpha sp., was chosen as a removed from the aquaria, patted dry and re­ chemically poor species (Pennings et al. 1993) and weighed to determine percentage consumption of was collected from the algal scrubbers at the JCU each alga (Palatability trial).

1 The genus Enteromorpha has recently been merged with the genus Ulva (Hayden et al. 2003). Throughout the present work 'Enteromorpha' has been used to designate the filamentous growth form of the genus Ulva. 14 c.L. Clarke

Statistical analysis 9 Descriptive length-frequency analysis was used to ~ 8 examine the population dynamics of the sea hare .~ 7 ~ W 6 population. Length-frequency analysis is a ~CJ) technique that examines changes in length of the cti -..!.. 5 ~} population, using a series of length histograms. 4 3l 'E 3 Length-frequency distribution reflects the c~ ell 2 interaction between rates of reproduction, growth, CD ~ 1 and mortality. Simple descriptive length-frequency o-1--::-=-5..J..Ju-n---"'-'-:7:-'-J~ul"'---'-::2-c'1 ""Ju"-I-':-27:-'J=u"'"l-'--3-::-S-ep---' analysis is used here to draw basic conclusions 2 about the characteristics of the population. More Sampling date formal length-frequency techniques could not be used because the full life history characteristics of 2 these species have not been tested. The sea hare Figure 1 The mean density (per m ) of Bursatella leachii lengths were divided into 5mm classes as this and Stylocheilus striatus within the seagrass beds of Shelly Beach in 2002. provided the best resolution of the patterns of recruitment and mortality. One-way ANOVA was transect area on 7th July 2002. Its density peaked at performed on the length of sea hares found during 0.88 individuals per m 2 and steadily declined in the each trip. following trips until no animals were recorded on 3 For the feeding preference trials, the autogenic September 2002. The mean density of S. striatus change calculated for each alga was used to correct th s th when present (7 , 21 t, and 27 July, 2002) was 0.42 the percentage consumption values (after Nicotri per m 2 (Figure 1). Formal analysis of the length of S. 1980; Peterson and Renaud 1989). Paired-samples t­ striatus was performed but is not included here tests were used to analyse the percentage because it did not illuminate any useful trends for consumption and behavioural choice data from this study. This may be a result of the relatively low each two-way choice trial. Where the data did not abundance recorded during most sampling trips. meet the assumptions of heterogeneity and normality a non-parametric Wilcoxon-signed ranks test was used to assess significance. Pulse settlement vs. continuous recruitment Evidence against a pulse settlement event is the mean size of each sampling trip. The sizes of B. RESULTS leachii found during each of the four sampling trips were significantly different (One-way ANOVA: df Aggregation characteristics = 3, F = 35.588, P < 0.001). There was a decrease in Sea hares were found in high abundance at Shelly mean length of B. leachii between 25 June and 7 Beach from 25 June to 27 July 2002. Two species of July, a small increase during 21 July and then sea hare were present: B. leachii and S. striatus. another small decline during 27 July (Figure 2). The Individuals of the two species were observed in the animals found on 25 June and 21 July were same areas, often in close association. A significantly similar in size and those in 7 July and cyanobacterial bloom was also present at Shelly 27 July were significantly similar in size (Tukey's Beach during the sea hare population irruption. The cyanobacterium was identified as C. crustacea (B. 60 Bendell, Jeu, pers. comm.) and was present both in A B A B ill' 50 ~ large tufts on the sediment and growing ,..-",- epiphytically on the seagrass leaves. i: 40 ~ E r-l<- During the initial sampling trip, 25 th June 2002, E :;; 30 only B. leachii was recorded in the transect area. The 0, c mean density of B. leachii at this time was 5.12 ~ 20 individuals per m 2 (Figure 1). The highest recorded c ~'" density of B. leachii was observed on 7 July when it 10 2 increased to 7.44 individuals per m and then 0 decreased in the subsequent sampling trips. No 25 Jun 17 Jul 21 Jul 27 Jul animals were recorded on the final sampling trip, 3 Sampling date September 2002. Throughout the entire month of sampling, the predominant species remained B. Figure 2 The mean length (mm +/- standard error) of leachii (Figure 1). The density of S. striatus was much Bursatella leachii individuals during the four sampling trips to Shelly Beach in 2002. The lower than that recorded for B. leachii for the letters denote significantly different sub­ duration of the population irruption. groups as determined by Tukey's HSD post­ Stylocheilus striatus was first recorded within the hoc tests. Population dynamics and feeding preferences of Bursu/dlu Il'ucllli 15

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Figure 3 lIt Bllr.',if,'II,) ICe/till I present at Beach In 2UU2 each l)t the four .cl Ijllh,anddi2711lh

! fSD post-hoc tests ~ubsl'ts A and B, SIN l!a~se~ the course of sampling 111 Figure Figure ThIS mdllates that then' \\,IS more than a 3. Thl're was also a gradual decline in the smglc settlement e\ent occurring at Shelh' Beach. abundance of larger size classes and the three There was continual recruitment ot smaller classes disappeared completely in the last indl\iduals mto the populatlOn at Shellv Beach sampling trip of. In late June 2002, the size classes during the sampling perIod 3) lhe small were normallv distributed with a peak at thl~ 50mm Sea hares grew larger and nW\'ed 111 to the lMgcr length class although there were slightlv more 16 CL. Clarke individuals in the larger size classes (Figure 3a). In early July, there was a peak of 40mm animals and two smaller peaks at 30 and 50mm. There were a high proportion of smaller individuals at this time (Figure 3b). There was an increase in the number of larger individuals sampled during the 21 July sampling trip (Figure 3c). At the end of July no one size class dominated the distribution and again there was an increase in the number of small individuals (Figure 3d).

Egg mass variation Sampling date The presence of characteristic string-like sea hare 2 egg masses within the sampling area indicated Figure 4 The mean density of egg masses (per m , +/­ spawning activity and the presence of standard error) found during each sampling trip within the seagrass beds of Shelly Beach reproductively mature sea hares. However, which in 2002. sea hare species had laid each mass could not be identified from the egg masses themselves in a field setting. The egg mass density during the 2002 sea including the cyanobacteria, C. crustacea. The mean hare population irruption peaked on July 7th (Figure percentage consumption, corrected for autogenic 4), which corresponds with the timing of the peak change, of each pair-wise trial is shown in Figure 5. in sea hare density (see Figure 1). The density of Only Enteromorpha and C. crustacea were consumed 2 egg masses at this time was 2.28 egg masses per m • in amounts greater than 10%. The feeding preference hierarchy of B. leachii was Enteromorpha Palatability sp. > C. crustacea> Sargassum sp. and P. pinnata. Bursatella leachii significantly preferred the green Enteromorpha was consumed significantly more than alga Enteromorpha over all other species tested, C. crustacea (Wilcoxon Signed ranks test: Z = -2.240,

---. W (f) i: 60 * * * * * ---c 50 o 'B. 40 ~ 30 (/) § 20 o ~ o 10 § 0 Q) ~

A B c o E F Algal Pairwise Trial

Figure 5 The mean percentage consumption (+/ - standard error) of each pairwise choice trial by BlIrsatella leachii. Asterisks (*) indicate significant choices as evidenced by the respective statistical test. Each colour code represents a single two-way choice experiment denoted by letters A-F where A = Enteromorpha sp. vs. Calothrix cnlstacea, B = Enteromorpha sp. vs. Pterocladia pillllata, C = Enteromorpha sp. vs. SargasSllnZ sp., D = Calothrix Cnlstacea vs. SargasslIm sp., E = Calothrix Cnlstacea vs. Pterocladia pimzata and F SargasslIm sp. vs. Pterocladia pinnata. Population dynamics and feeding preferences of Bursatel/a lcacilii 17

P OJ)25), Sargasslll11 (Wilcoxon signed ranks test: Z algae presented to B. Icae/lii had at least one -2.100, P (HB6) and P. pilllzata (Wilcoxon signed individual found upon it at least once during the ranks test: Z -2.521, P 0.012). Calotllrix crustacea trials. was consumed significantly more than Sargassum sp. (Wilcoxon signed ranks test: Z = -2.521, P 0.012) and P. pinnata (Wilcoxon signed ranks: -2.521, DISCUSSION p 0.(12). There was no significant difference between the consumption of SargasslIIll sp. and P. Sea hare density pinnata (Wilcoxon signed ranks test: Z = -1.400, The sea hare population at Shelly Beach reached p>0.(5). extremely high densities during the sampling period compared to those previously reported Attractiveness (Carefoot 1987). In June 2003, another population The presence of individual sea hares on each alga irruption event was documented at the same yielded almost the same feeding preference location (Clarke 2(04) where S. striatus reached high 2 hierarchy as that obtained by the direct measure of density (3.84 per m ) while B. leaclzii was found at 2 percentage consumption: Entcromorplza sp. > C. lower density (0.24 per m ). Styloelzeilus striatus has crustacea> P. pinnata and Sargassurll sp. The place of been reported in large numbers in association with P. pinnata and Sargassul11 sp. were reversed in this blooms of Lyngbya majuscllla in Hawaii (Switzer­ data set but there was no significant difference Dunlap and Hadfield 1979) and Guam (Paul and between the two. The mean number of times a sea Pennings 1991; Nagle et al. 1998) but the densities hare was present on each alga during the pair-wise were never quantified. Lowe and Turner (1976) trial is shown in Figure 6. Bllrsatclla leaclzii was reported substantially higher densities of B. leachii recorded significantly more on Enterol11orplw than in Florida. However, the density reported for C. crustacea (Wilcoxon signed ranks test: Z = -2.058, subtidal populations was based on the number of P 0.(40) or P. pinnata (Wilcoxon signed ranks: Z animals within a single aggregation. Other sea hare -2.251, P 0.(24). Bllrsatclla Imelzii significantly species have much lower densities than those preferred C. crllstacea over P. pinnata (Wilcoxon recorded here. Carefoot (1987) reviewed the signed ranks: Z -2.041, P = 0.(41). Each of the four reported densities of several species of Aplysia and

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Figure 6 The mean number of times Bursatel/a leacl1l1 was recorded present on each alga within in each pairwise trial. Asterisks (*) mdicate stahshcally significant differences. Each colour code represents a single two-way chOiCe expenment denoted letters A-F where A Ellterolllorpha sp. vs. Calotilrix crustacea, B Entcrolllorpha sp vs. Pterocladla C. sp. vs. sp., D Calothrix crustacea vs. SargasslIlIl sp., E Calothnx crllstacea vs. Ptcrocladla and F sp. vs. Ptcrocladza pll/llata. 18 c.L. Clarke

the average densities never exceeded 5.0 per m 2 the one that is the most consumed. Stylocheilus with most reports less than 1 per m 2 (Willan 1979; striatus has only been reported to feed upon L. Carefoot 1987). The low densities of Aplysia species majuscula overseas (Switzer-Dunlap and Hadfield have often been used as evidence for the limited 1977; Paul and Pennings 1991; Nagle et at. 1998). role of all sea hare species in the marine community Though S. striatus and B. leachii seem to be common (Carefoot 1987; Rogers et al. 2003). However, the together, B. leaclzii is reported to feed on a number present study indicates much higher densities for B. of red and green algae. The reason for the greater leachii than the members of the more commonly dietary range of B. leachii has not been previously studied genus Aplysia. discussed yet recent work on the way these two sea hares digest chemically rich foods has been Aggregation of sea hares on cyanobacterial conducted. Capper (2003) showed that there are blooms differences in the way B. leachii and S. striatus deal The co-occurrence of B. leachii and S. striatus and with the secondary metabolites present in L. the bloom of the cyanobacterium, C. crustacea in majuscula. B. leachii excretes secondary metabolites 2002 has not been documented previously. At the in the ink and faecal matter while S. striatus stores same location in a subsequent year these sea hare these metabolites in the digestive gland. The species were associated with a different strategies of these two co-occurring species thus unidentified cyanobacteria species (Clarke 2004). differ; S. striatus may have specialized to deal with Bursatella leachii is believed to have a more catholic the specific metabolites of L. majuscula while B. diet than S. striatus (Wu 1980; Paige 1988). In Hong leachii excretes the chemicals and thus is more likely Kong, B. leachii consumes a range of macroalgae, to be able to deal with a larger range of metabolites preferring Enteromorpha prolifera, although than S. striatus (Capper 2003). cyanobacteria species were not tested (Wu 1980). In Preferred choices may not offer the best long-term Florida, only species of cyanobacteria (including L. growth and fitness. Aplysia punctata consumes majuscula) were preferred in food choice tests and Enteromorpha sp. preferentially in the laboratory but as metamorphic substrates (Paige 1988). In contrast, animals on a diet of the red alga, Plocamium sp., all previous reports have linked S. striatus with L. have lowered faecal production and better growth majuscula, its preferred food according to a number (Carefoot 1967). Monospecific diets of preferred of authors (Paul and Pennings 1991; Pennings et al. chemically rich species have shown increased 1996; Nagle et al. 1998). mortality for B. leachii and S. striatus (A. Capper, During the present study, B. leachii preferred the pers. comm.) and for A. parvula (Rogers et al. 1995). green alga, Enteromorpha sp., to the cyanobacterium The next step in investigating the feeding C. crustacea, the brown macroalga Sargassum sp., preferences of B. leachii would be to compare the and the red macroalga P. pinnata. Enteromorpha sp. long term growth and reproduction of animals fed was preferred even to the cyanobacterial species (c. Enteromorpha sp. with those fed cyanobacteria. crustacea) that the animals were seen to be feeding upon in the field. The occurrence of Enteromorpha Population irruption dynamics sp. was extremely rare at the sampling site. Several The length-frequency distribution of this sea hare species exhibit greater generalization of population can be used to investigate hypotheses feeding preferences in the laboratory than are about its dynamics (see Gev et al. 1984). It is exhibited in the field (Saito and Nakamura 1961; important to note that length-frequency analysis is Winkler and Dawson 1963; Carefoot 1987; Rogers et based on the assumption that length is a reasonable al. 2003). For example, some members of the genus proxy for age. A single study found that length and Aplysia are often considered to specialize on red age are directly related for B. leachii although only a algae in the field (Carefoot 1987) and yet laboratory small number of animals were used in experiments experiments have repeatedly shown their (Willan 1979). Other molluscs shrink under preference for green algae (Winkler and Dawson conditions of stress or low food availability 1963; Rogers et at. 2003). Winkler and Dawson (Russell-Hunter et al. 1984; Russell-Hunter 1985). (1963) found that A. californica were only inhabiting This is unlikely in the present study because the red algae in the field, but preferred Enteromorpha in concurrent cyanobacterial bloom provided an laboratory testing. Additionally, Saito and abundance of food, at least for the majority of the Nakamura (1961) found that A. juliana and A. sea hare population irruption event. The hypothesis kurodai consumed species of brown and red algae being tested was that sea hare population irruptions respectively in the field but both preferred species are the result of settlement of a single cohort on the of Enteromorpha and Ulva in the laboratory. cyanobacterial bloom. Similar studies with co­ The feeding preference hierarchy of B. leachii was occurring Aplysia depilans and Aplysia fasciata in identical whether obtained by testing palatability or Israel showed a single recruitment pulse (Achituv attractiveness. Therefore the alga that individual sea and Susswein 1985). If a single pulse occurred we hares chose to inhabit (the most attractive) was also would expect that the length-frequency analysis Population dynamics and feeding preferences of Bursatella leachii 19 would have detected a large cohort of animals of population dynamics of B. leachii and S. striatus in similar size moving through the size classes. This Shelly Beach. did not seem to be the case here, because for B. The other possibility for the observed depletion of leachii, there was a continual addition of small large sea hares is migration. If the animals were recruits. In conjunction, there were also a small migrating to areas unavailable to observation then number of individuals in the large size classes. we would expect to see an abrupt appearance or Thus, the size distribution of this population disappearance of mature animals. The continual indicates that recruitment of individuals into the recruitment of small B. leachii into the population in population is occurring throughout the duration of 2002 rules out the possibility that this high-density the cyanobacterial bloom. occurrence was merely a roving population of Additionally, if the sea hare population irruption adults. It would be expected that migration would was a pulse-recruitment event we would expect to cause an increase/decrease in abundance of all size see a gradual increase in size and then an abrupt classes, which was not observed here. There was a end to the population. The mean length of B. leachii gradual decline of the number of large animals over was not significantly different through the duration time, suggesting that a mass migration was not the of the cyanobacterial bloom. Thus, the animals were cause of the disappearance of sea hares in this similar in size or size range throughout their population. This gradual decline is suggestive of a presence in the seagrass beds. The presence of egg natural senescence of older sea hares, especially masses over the entire seven-week period also when it is considered that the timing of the suggests that the population in Shelly Beach was population irruption event is comparable to the not the result of a single recruitment pulse. Egg three month life span of B. leachii (Paige 1988). masses indicate the existence of reproductively The large amount of cyanobacteria biomass mature and active adults within the population at observed at Shelly Beach would provide a sizeable all times. Aplysia species have been reported to area for settlement. In Florida, B. leachii preferred to restrict reproductive activities to certain habitats settle on three species of cyanobacteria, L. majuscula, and certain seasons (Willan 1979; Carefoot 1987). Schizothrix calciola and Porphyrosiphon notarisii For example, Willan (1979) found that the intertidal (Paige 1988). In Hawaii, L. majuscula is known to area he studied only contained immature Aplysia serve as a preferred site of settlement for S. striatus, dactylomela and therefore no egg-laying occurred. along with a small number of red algae species The presence of sea hares from a wide size-range (Switzer-Dunlap and Hadfield 1977). The physical and the observed egg masses indicates that this conditions that promote cyanobacterial blooms may population contained both immature and also be favourable for the influx of sea hare larvae reproductively mature sea hares at the same time into Shelly Beach seagrass beds. In addition, the and therefore was not the result of a pulse ability of sea hare larvae to move towards chemical recruitment event. cues for settlement is currently unknown but if they Large adults that were lost throughout the possess a certain degree of swimming ability (as duration of the cyanobacterial bloom were either seen in reef fish larvae Fisher et al. 2000), these removed from the population by mortality, cyanobacterial blooms may send out strong signals migration, or natural senescence. Decreasing into the water column for larvae to orient towards. abundance of cyanobacteria could cause starvation­ The consumption of epiphytic cyanobacteria by induced mortality. Mortality could also be caused large numbers of sea hares may aid in maintaining by predation. Nassarius sp. snails were observed the seagrass community composition. Sea hare feeding upon sea hare carcasses although it is grazing removed epiphytic cyanobacteria from unknown whether this predator caused the death of seagrass blades. If seagrass blades become the animals or were merely scavenging. Other overgrown by epiphytes, sunlight is blocked and predators may move into the study area with high dieback may occur (Lubchenco and Gaines 1981). tide, which renders the area unavailable for study. The sea hares did not completely consume the site's A small number of predators have been shown to cyanobacteria biomass in this instance. However, regularly prey upon sea hares and the species differ the seagrass community likely derived some benefit between systems. Known sea hare predators from the short-lived sea hare irruption. include the sea anemone Anthopleura xanthogrammica in California (Winkler and Tilton 1962), the pycnogonid Anoplodactylus evansi in CONCLUSIONS temperate Australia (Rogers et al. 2000), the sea star The sea hares B. leachii and S. striatus were found Coscinasterias calamaria in New Zealand (Willan at densities far greater than those previously 1979) and the gastropods Navanax and Melo amphora reported for other sea hare species. This suggests (Pennings 1990a; Johnson and Willows 1999). It is that these sea hare species may be important unknown at this time whether natural predation consumers of the sporadic cyanobacterial blooms events are an important source of mortality for the that occur in sea grass beds and other coastal 20 c.L. Clarke habitats. Analysis of the population dynamics Carefoot, T. H. (1967). Growth and nutrition of Aplysia revealed that the population irruption observed punctata feeding on a variety of marine algae. Journal was not the result of a pulse recruitment event, but ofthe Marine Biological Association ofthe United Kingdom rather a continuous supply of recruits, in contrast to 47: 565-589. previous studies. Techniques such as population Carefoot, T. H. (1970). A comparison of absorption and genetics and larval tows are needed to shed further utilization of food energy in two species of tropical light on recruitment patterns in this ecosystem. Aplysia. Journal of Experimental Marine Biology and Ecolog1j 5: 47-62. The difference between the preferred alga in the Carefoot, T. H. (1987). Aplysia: its biology and ecology. laboratory and the prey species that was B. leachii Oceanography and Marine Biology Annual Review 25: feeding upon in the field reflects the complications 167-284. associated with attempting to separate the various Clarke, c.L. 2004. The ecological role of sea hares factors influencing feeding preferences in sea hares. (Opisthobranchia: Anaspidea) within tropical intertidal It seems that the most important factors dictating habitats. MSc Thesis. James Cook University, feeding preferences in B. leachii are the palatability, Townsville, Australia. 141 pp. abundance in the natural habitat, and though not Coleman, N. (2001). 1001 Nudibranchs: Catalogue of Indo­ directly tested here, likely the secondary chemistry Pacific Sea Slugs. Neville Coleman's Underwater of the food item. The demonstrated ability of B. Geographic Pty Ltd, Springwood, Qld. leachii to reach large population sizes while feeding Colgan, M. W. (1987). Coral reef recovery on Guam, on a sub-optimal food source highlights the Micronesia after catastrophic predation by Acanthaster flexibility of feeding in these sea hares. The planci. Ecolog1j 68(6): 1592-1605. plasticity in feeding is likely to enhance the ability Cote, I. and Reynolds, J. D. (1998). Tropical fish: of sea hares to successfully exploit an abundant, but ExplOSions and extinctions. Trends in Ecology and often, unpredictable resource. The aggregations of Evolution 13(12): 475-476. B. leachii observed at Shelly Beach, Townsville are Crawley, M. J. (1983). Herbivory: The Dynamics ofAnimal­ not the result of single pulse recruitment. The Macrophyte Interactions. Blackwell Scientific Publications, Oxford. evidence presented here suggests that the Fisher, R., Bellwood, D. R. and Job, S. D. (2000). aggregations were supported by continual Development of swimming abilities in reef fish settlement in response to what may be a less than larvae. Marine Ecology Progress Series 202: 163-173. ideal food source. Gev, 5., Achituv, Y. and Susswein, A. J. (1984). Seasonal determinants of the life cycle in two species of Aplysia ACKNOWLEDGEMENTS found in shallow waters along the Mediterranean This work was completed as part of the MSc. coast of Israel. Journal of Experimental Marine Biolog1j degree program at James Cook University. The and Ecology 74: 67-83. author would like to thank Gilianne Brodie, Rocky Ginsburg, D. W. and Paul, V. J. (2001). Chemical defenses in the sea hare Aplysia parvula: importance of diet and de Nys and Annette Klussmann-Kolb for their sequestration of algal secondary metabolites. Marine supervision. Financial support was provided by Ecology Progress Series 215: 261-274. CRC Reef, the Malacological Society of Australasia Hay, M. E., Pawlik, J. R., Duffy, J. E. and Fenical, W. and James Cook University. Laboratory work was (1989). Seaweed-herbivore-predator interactions: host­ performed at the MARFU aquarium facilities at macrophyte specialization reduces predation on small James Cook University. Two anonymous reviewers herbivores. Oecologia 81: 418-427. provided valuable advice on an earlier version of Hayden, H.5., Blomster, J., Maggs, C. A. Silva, M.J. this manuscript. Stanhope, and Waaland, J. R. 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