Diurnal observations of sheltering behaviour in the coral reef sea cucumber Holothuria whitmaei

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Fisheries Research 91 (2008) 112–117

Short communication

Diurnal observations of sheltering behaviour in the coral reef sea cucumber Holothuria whitmaei Glenn R. Shiell ∗ , Brenton Knott Animal Biology (MO92), The University of Western Australia, 35 Stirling Hwy, Crawley, Perth, WA 6009, Australia Received 7 July 2007; received in revised form 13 December 2007; accepted 13 December 2007

Abstract Management of commercial sea cucumber stocks relies, in part, on estimates of population densities which, in-turn, depend on knowledge of habitat preferences, and of the influence of biological cues on sheltering and/or aggregation behaviour. Here, we document a diurnal shift in the sheltering behaviour of the Pacific and eastern Indian Ocean black teatfish, Holothuria whitmaei, and discuss the implication of this behaviour for surface-based population density surveys. Diurnal studies of 30 black teat fish on Ningaloo Reef, Western Australia, found that the proportion of animals sheltered (and therefore hidden when viewed from directly above) was significantly greater in the morning (3–23%; AM 0830-1230 h) relative to the afternoon (0–6%; PM 1230-1730 h). As with sheltering behaviour, the straight-line distance between individual sea cucumber and the nearest shelter also showed marked diurnal variation, with animals observed at greater distances from shelter between 1230 and 1730 h (PM 4–22 cm; AM 1–7 cm). Based on these results, we suggest that surfaced-based census techniques (e.g. manta tows) may underestimate population densities if conducted during times of reduced activity and increased incidence of sheltering behaviour. Appropriate calibration factors for day-time black teatfish surveys are proposed. © 2007 Elsevier B.V. All rights reserved. Keywords: Holothuria nobilis; Fisheries; Censusing; Bˆeche-der-mer; Trepang

1. Introduction Despite the ecological significance of coral reef dwelling sea cucumbers (Bakus, 1973; Aller and Yingst, 1985; Amon and Herndl, 1991; Uthicke and Klumpp, 1998; Uthicke, 1999, 2001a,b), wild populations are subjected currently to unprecedented levels of commercial exploitation (Rees et al., 2003; Altamirano et al., 2004). One species of particular commercial interest, and therefore one that is impacted heavily, is the Pacific and eastern Indian Ocean black teatfish Holothuria (Microthele) whitmaei Bell 1887. This economically valuable species has been fished to the point of near local extinction in NW Australia (Rees et al., 2003) and harvested in sufficient quantities from the Great Barrier Reef, Queensland (NE Australia), to result in the closure of the fishery in the late 1990s (Uthicke and Benzie, 2000). Further, and of greater concern, is that this species is now

∗ Corresponding author at: Oceanica Consulting Pty Ltd., 99 Broadway, Nedlands, Perth, WA 6009, Australia. Tel.: +61 8 9389 9669; fax: +61 8 9389 9660. E-mail address: [email protected] (G.R. Shiell).

0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2007.12.010

recognised as a separate species from the western Indian Ocean black teat fish (H. nobilis); hence, its distribution, and therefore its overall abundance, is more limited than thought previously (Uthicke et al., 2004). Increasing demand for sea cucumber, together with evidence of a world wide decline in natural stocks (Conand, 2004), suggests that management of wild sea cucumber fisheries is now more important than ever. Effective management relies, in part, on knowledge of natural population densities prior to fishing, and an estimation of minimum densities expected to overcome the limitations of the Allee effect i.e. the minimum densities expected to maintain fertilisation success between individuals (Levitan, 1991; Levitan and Petersen, 1995). However, gathering density data is rarely straightforward, as the distribution of sea cucumbers is often patchy, leading to significant sample variation when surveys cover large areas (Bell and Nash, 2004). Indeed, censusing has the potential to underestimate or overestimate the density of a given population, depending on the scale of the habitat included in the survey. In addition, there is relatively little information available on the specific habitat preferences of many species, or of the influence of biological cues on the incidences of species aggregations. For this reason, the importance

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of standardised census techniques based on knowledge of habitat preferences is acknowledged (e.g. Conand, 2004). However, the accuracy of surface-based population surveys is dependant also on biological knowledge of the target species, including, knowledge of diurnal sheltering behaviour (Lovatelli et al., 2004). Cryptic or sheltering behaviour in holothurians is well documented in the literature (e.g. Yamanouchi, 1956; Berrill, 1966; Hammond, 1982; Graham and Battaglene, 2004). Yamanouchi (1956) suggested that aspidochirote holothurians can be classified into those that shelter during periods of reduced feeding activity (e.g. Holothuria thomasi, Actinopyga agassizi, Euapta lappa and Stichopus chloronotus), and those that remain visible whilst feeding continuously (e.g. Holothuria mexicana, H. atra, H. edulis, H. flavomaculata and Isostichopus badionotus) (see also Hammond, 1982). Anecdotal observations of the Pacific and eastern Indian Ocean black teatfish on Ningaloo Reef, Western Australia, found consistently higher numbers of animals beneath coral (or other obscuring structures) between 0600 and 1100 h. Consequently, we monitored the behaviour of H. whitmaei on Ningaloo Reef, Western Australia, to (a) confirm the validity of the sheltering observations, and (b) determine the

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extent to which this behaviour may compromise the accuracy of population density estimates. 2. Methods Densities of the Pacific and eastern Indian Ocean black teatfish on Ningaloo Reef are greatest on the outer reef flat where they are found typically upon sand among coral heads and scattered coral rubble (Shiell, 2004). For this study, 30 adult black teatfish were collected from reef flat and divided equally among five study sites, all distributed upon similar reef flat habitat within an area of approximately 1000 m2 (Fig. 1). Each of the five sites had near-identical physical habitat characteristics, namely, linked expanses of sand, coral rubble and numerous coral heads. Where it was not possible to locate specimens within the study area (Fig. 1), individuals were translocated from adjacent areas of reef flat, but never from distances greater than 100 m. For identification, each animal was marked with a number (following the methods of Reichenbach, 1999; Mercier et al., 2000) and left to recover for at least 5 days; the period required for marked specimens to elicit rates of activity statis-

Fig. 1. Line drawing: Location of study area and surrounding habitat structures. Aerial photograph: Details of the study area located approximately 3 km SW of Coral Bay, Ningaloo Reef, Western Australia.

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tically equivalent to control specimens (Shiell, 2006). For ease of diver navigation, the boundaries of the study sites were connected with submerged string lines, and the position of animals indicated by coloured plastic tape attached to the nearest hard object. 2.1. Diurnal sheltering behaviour Sheltering behaviour was monitored over five consecutive days in August, 2003. Observations were conducted on each of the 5 days over four 2-h time periods, namely: early-morning (EM; 0830 to 1030 h); mid-morning (MM; 1030 to 1230 h); mid-afternoon (MA; 1230 to 1530 h); and late-afternoon (LA; 1530 to 1730 h). At the beginning of each period, all animals were located by SCUBA and then an observer at the surface of the water assigned one of three ‘visibility’ categories, each based on the visual criteria listed in Table 1. All observations of sea cucumbers were made by the same observer from a vertical distance of 5–6 m (depending on the tide). Although three visibility categories were included in the field study, here we combined for analysis the ‘near shelter’ and ‘on open sand’ categories to form an overarching ‘visible’ category. This was considered necessary since, in the case of ‘near shelter’, the animals remained ‘visible’ to the observer and therefore, were likely to be recorded by a trained observer. In the same context, results are presented primarily for the ‘hidden’ category, since ‘hidden’ and ‘visible’ are reciprocal to one another. For statistical analysis, data were combined to yield two periods of observation: AM (0830–1230 h) and PM (1230–1730 h). The number of ‘hidden’ animals over the 5-day period was pooled, such that for both the AM and PM monitoring periods, each site yielded a total of 30 observations i.e. six animals × five daily observations. Differences in the number of animals ‘hidden’ between the AM and PM monitoring periods were analysed with a paired t-test (SPSS V11.5). 2.2. Distance between H. whitmaei and potential shelter In addition to assigning visibility categories to individual animals, we considered also the straight-line distance between each of the animals and the nearest available shelter. The straightline distances (cm) between each of the animals and their nearest available shelter were determined across each of the daytime intervals: early-morning (EM; 0830–1030 h); mid-morning

(MM; 1030–1230 h), mid-afternoon (MA; 1230–1530 h) and late-afternoon (LA; 1530–1730 h). Using a flexible measuring tape, divers measured the straight-line distance between the nearest coral habitat and the edge (nearest to that of the habitat) of the animal’s body. Care was taken not to make contact with the animal during this process, as physical disturbances resulted typically in the retraction of the feeding tentacles √ and a short period of inactivity. Straight-line distances were x + 1 transformed (homoscedasticity achieved and confirmed with Levene’s test) and compared across each of the day-time periods using a repeated measures two-factor ANOVA. The two-fixed factors were time of day (T-within subjects repeated measures factor with four levels) and site (S-between subjects factor with five levels). ANOVA and pair-wise post hoc procedures were performed using SPSS V11.5 software. 3. Results 3.1. Diurnal sheltering behaviour Diurnal monitoring of 30 individual Holothuria whitmaei specimens revealed a significant shift in sheltering behaviour, with higher proportions of animals in the ‘hidden’ state prior to midday (Fig. 2). Between 0830 and1230 h (AM), 3.3–23.3% of animals were classified as ‘hidden’. By contrast, the proportion of animals classified as ‘hidden’ between 1230 and1730 h (PM) was significantly lower at between 0 and 6.7%; particularly late in the afternoon (LA; 1530–1730 h) when the proportion was ≤3.3% at four of the five sites. Hidden, specimens were typically inactive with their feeding tentacles retracted; specimens in the open were observed typically with their feeding tentacles extended. The extent to which the number of ‘hidden’ animals differed between AM and PM monitoring periods was analysed with a paired t-test. Data used in this analysis, along with the number of animals assigned to the ‘visible’ category, are presented in Table 2. These data, together with the highly significant t-test result (t = 4.894, p = 0.008), indicate that the proportion of ‘hidden’ animals is greater in the morning relative to the afternoon (PM). 3.2. Distance between H. whitmaei and potential shelter The straight-line distance between individual specimens and the nearest coral habitat varied depending on the time of day. H. whitmaei were situated closer to shelter in the early to mid-

Table 1 Criteria used to assess visibility categories Category

Visibility criteria (when viewed from directly above)

1

Hidden

2

Near shelter (visible)

3

On open sand (visible)

Where the entire body of the animal was hidden beneath obscuring habitat such that a snorkeller positioned directly above at 90◦ could not see any portion of the animal Where an animal was partly obscured, or positioned on, or immediately adjacent to coral habitats, reflecting circumstances in which an animal may be difficult to observe due to the obscuring effect of overhanging plate coral Where the entire animal was observed in the open on bare sand at a distance of at least one body length from coral habitat, and well away from potential obscuring habitat

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Table 2 Number of animals classified as either ‘hidden’ or ‘visible’ in the morning (AM) and afternoon (PM) observation periods Period

Site

Number of animals assigned to visibility category Visible

Hidden

% Hidden

AM

1 2 3 4 5

48 (43) 48 (41) 57 (49) 48 (39) 50 (45)

12 12 3 12 10

20.0 20.0 5.0 20.0 16.7

PM

1 2 3 4 5

59 (38) 58 (44) 59 (39) 57 (30) 57 (42)

1 2 1 3 3

1.7 3.3 1.7 5.0 5.0

‘Visible’ includes pooled observations for ‘near shelter’ and ‘on open sand’. Numbers in parenthesis are the number of animals assigned to the ‘near shelter’ category. Sixty observations are represented i.e. 6 animals × 5 days × 2 monitoring periods (EM&MM and MA&LA).

Fig. 2. Diurnal incidences of the proportion of H. whitmaei specimens classified as ‘hidden’ in August, 2003. Data are presented for 4-time categories: earlymorning (EM); mid-morning (MM); mid-afternoon (MA) and late-afternoon (LA). Values in histograms represent percentage of animals derived using combined results over 5 days (30 observations per site).

morning periods, when animals were, on average, 1–7 cm from the nearest physical habitat. In contrast, animals were on average situated between 4 and 22 cm from shelter in the late-afternoon period (Fig. 3). Statistical analysis (ANOVA) determined that the straightline distance between specimens and the nearest coral habitat differed significantly between the four monitoring periods (p < 0.001). The subsequent post hoc procedure determined that the distance between individual specimens and shelter was significantly less in the EM and MM periods, relative to the EA and LA periods (Table 3). No significant differences (p = 0.631) were detected between the two morning observation periods (i.e. EA and MM) and, similarly, no significant difference (p = 0.669) was detected between the two afternoon periods (i.e. MA and LA). In addition, no significant differences were detected among sites, suggesting the observed patterns were consistent on a spatial scale (Table 3).

Fig. 3. Mean distances (cm) of H. whitmaei from nearest available shelter in August, 2003. Four time periods are represented: () early-morning (EM); ( ) mid-morning (MM); ( ) mid-afternoon (MA) and ( ) late-afternoon (LA). For each of the monitoring periods, histograms are arranged top to bottom from sites 1–5, respectively (averages based on the combined results for 5 days; 30 observations per site).

4. Discussion 4.1. Sheltering behaviour Cryptic or sheltering behaviour in holothurians is typically reported in nocturnal holothurians (Yamanouchi, 1956; Hammond, 1982; Pawson and Caycedo, 1980); but few comparable data exist for aspidochirote species that forage actively during day-light hours, as suggested here for Holothuria whitmaei. Excluding the behaviour of burrowing species (Mercier et al., 2000), only Actinopyga mauritiana (Graham and Battaglene, 2004), Stichopus chloronotus and Stichopus variegatus (now S. herrmanni) (Yamanouchi, 1956; Uthicke, 1994) maintain some form of concealment during periods of reduced activity.

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Table 3 Results of the two-factor repeated measures ANOVA and pairwise post hoc procedures assessing the effect of time of day (T) and site (S) on the animal’s distance from shelter during August, 2003 Sources of variation Within subject effects Time of day (T) Time × site (T × S) Residual Between subject effects Site (S) Residual

d.f.

MS

F

p

3 12 75

26.763 1.657 1.703

15.71 0.973

< 0.001 <0.482

4 25

3.562 5.298

0.672

<0.617

Post hoc pairwise comparison

EM, MM, MA and LA represent early-morning, mid-morning, mid-afternoon and late-afternoon, respectively. For the post hoc comparison, monitoring periods that are not statistically different from one another are joined by an underlying horizontal bar (as in the case of EM and MM)

It is not clear why up to 23% of H. whitmaei specimens were hidden from some time during the night until midday. Monitoring of sheltering behaviour began 5 days following marking, so it is unlikely the behaviour resulted from stress associated with initial handling (Shiell, 2006). Given that observations of sheltering behaviour were limited to August, 2003, it is possible that the results were confounded by water temperature. However, previous unpublished observations of the same study group in January and April observed similar behavioural trends to those reported here, with specimens tending to remain hidden in the morning period before emerging around midday. The behaviour may reflect a phylogenetic carry-over from ancestral holuthurians (sensu Hammond, 1982), or it may reflect predator avoidance; however, adult H. whitmaei have few, if any predators. Francour (1997) provides an exhaustive review of predation on holothurian and lists crustaceans, gastropods, asteroids, fish, birds and mammals as predators. Although many such predators frequent reefs inhabited by H. whitmaei, this species has yet to be documented as natural prey to any of the predators listed here. 4.2. Implications for surface-based population census methods The surface-based rapid assessment survey method of manta towing is a useful technique for estimating broad-scale changes in population densities of benthic animals (Fernandes et al., 1990; Moran and De’ath, 1992). Uthicke and Benzie (2000) and Benzie and Uthicke (2003) used manta tows extensively to measure densities of H. whitmaei, after initial trials indicated that densities were too low to be estimated efficiently with traditional line transects (Uthicke and Benzie, 2000). A typical manta tow survey, involving approximately 50–60 manta tows, is capable of detecting a 20% change in the abundance of crown of thorns starfish Acanthaster planci (Moran and De’ath (1992). Given that the difference in the proportion of specimens hidden between the early-morning (EM) and late-afternoon (LA) monitoring periods was at least 20% at three of the five study sites, manta tows may be sufficiently sensitive to detect changes in population densities of H. whitmaei between these periods. Nevertheless, the ability to detect a 20% change may be compromised by variation in population densities, differing survey techniques, observer bias (Fernandes et al., 1990) and inclusion of inappropriate habitat (Bell and Nash, 2004). It is also

acknowledged that densities reported for H. whitmaei (Massin and Doumen, 1986; Conand, 1989, 1990; Lokani, 1990; Preston, 1993; Long et al., 1996; Lawrence et al., 2004; Byrne et al., 2004) differ by margins greater than 20%, and that differences in locality and/or survey technique alone may contribute more error than sheltering behaviour. Consequently, without rigorous testing, it is uncertain whether the experimental results presented here may translate into similar findings when conducting manta tow surveys at different times during the day. Nevertheless, we estimate that sheltering behaviour may contribute to the underestimation of population densities by as much as 16% in the morning, and 3% in the afternoon. Although conservative, these values (derived simply by calculating the average number of animals ‘hidden’ in the morning versus afternoon) may serve as appropriate calibration factors for day-time black teatfish surveys. The ever-increasing commercial exploitation of holothurians, together with improved knowledge of habitat preferences (Uthicke and Benzie, 2000; Shiell, 2004), is likely to result in further, more extensive population density surveys centred over appropriate habitat. Hence, it is reasonable to assume that, with time, the accuracy of density estimates will improve and, as a result, errors associated with diurnally variable patterns of sheltering behaviour in H. whitmaei may become increasingly important. This notion is congruent with similar concerns expressed by Graham and Battaglene (2004) who suggested that sheltering behaviour in A. mauritiana may confound abundance surveys, if such techniques are conducted whilst animals are sheltering, and thus invisible to a surface-based observer. Acknowledgements We acknowledge the financial assistance provided by Oceanwest Fisheries, Exmouth, and the support of Mr. Barry Elliott. Additional funding for the study was provided by an Australian Research Council Post Graduate Award (Industry) to BK and the School of Animal Biology, The University of Western Australia. Original versions of the manuscript benefited from comments and suggestions by K¯aren Crawley, and later versions from two anonymous referees. Hamish Maitland and Nathalie Malo are acknowledged for invaluable field assistance. All data were collected according to Western Australian Government

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