zonation, behaviour and morphology of the intertidal coral-treader hermatobates (hemiptera:...
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<oological Journal of the Linnean Sociefy (1989), 96: 87-105. With 10 figures
Zonation, behaviour and morphology of the intertidal coral-treader Hermatobates (Hemiptera: Hermatobatidae) in the south-west Pacific
W. A. FOSTER, F.L.S.
Department of ,zbology, University of Cambridge, Downing Street, Cambridge CB2 3EJ
Received June 1988, accepted f o r publication October I988
The coral-treaders (Hermatobatidae) are the only exclusively marine family of insects. Observations in the Cook Islands, Samoa, Tonga and Fiji show that the insects can be abundant on shores that provide rocks with cavities that remain air-filled during high tide. The zone of suitable habitats for the insects is restricted to a narrow (c. 20 cm) vertical band roughly centred around Mean Low Water Neaps. Transplant experiments show that the insects are unable to survive above or below this zone. The insects emerge from their rocky crevices about an hour before low tide, swim on the water surface during low tide, and return to their crevices about an hour after the tide has turned. There are only four larval instars, which can be readily separated by their morphology. Electron microscope studies show that the insects are clothed in a layer of micro-hairs of unique design: a short tapering shaft tipped with a sphere. These micro-hairs may act as a plastron: their distribution corresponds precisely to the pattern of the silvery ‘air-layer’ seen when the insects are submerged, their spherical tips provide a regular array that could support an air-water interface, they occur at high densities (up to 3.5 x 106 mm-?), and the layer makes connection with the thoracic spiracles. Half the insects were able to survive submergence in recirculated seawater for 12 hours. The adults appear to swim further from shore than the larvae, and they were observed copulating in tidal pools.
KEY WORDS:-Hermatobates - Gerromorpha - marine insect - plastron - south-west Pacific.
CONTENTS
Introduction . . . . . . . . . . . . . . . . . . . . 88 Material and methods. . . . . . . . . . . . . . . . . . 88
Systematics . . . . . . . . . . . . . . . . . . . 88 Study sites . . . . . . . . . . . . . . . . . . . 88 Methods . . . . . . . . . . . . . . . . . . . . 89
Results . . . . . . . . . . . . . . . . . . . . . 9 0 Biometry and instar determination. . . . . . . . . . . . . . 90 Anatomy. . . . . . . . . . . . . . . . . . . . 93 Submergence experiments . . . . . . . . . . . . . . . . 97 Distribution . . . . . . . . . . . . . . . . . . . 98 Activity during the tidal cycle. . . . . . . . . . . . . . 100 Observations on feeding, moulting and mating . . . . . . . . . . 101
Discussion. . . . . . . . . . . . . . . . . . . . 102 Acknowledgements . . . . . . . . . . . . . . . . . 104 References . . . . . . . . . . . . . . . . . . . 105
87 0024-- 4082/89/050087 + 19 $03.00/0 01989 The Linnean Society of London
88 W. A. FOSTER
INTRODUCTION
Although most intertidal animals are of marine origin, a diverse array of animals has invaded the intertidal zone from land and freshwater. These animals are of interest because the problems that confront them are sharply contrasted with those faced by marine animals: seawater, not air, is the alien medium, and the environment is most harsh at the lower, rather than the higher, zones on the shore. Probably no other group of freshwater animals has been more successful in colonizing the intertidal zone than the semiaquatic bugs or Gerromorpha (Hemiptera), which include the familiar pondskaters and water crickets. Fourteen of the 120 genera of Gerromorpha occur in marine environments, and there have been at least eight independent invasions of the intertidal zone (Andersen, 1982). The semiaquatic bugs are of particular interest because they include the only insects (Halobates), of the million or so described species, that have successfully colonized the open oceans (Cheng, 1985).
The Hermatobatidae, which include the single genus Hermatobates, are the only exclusively marine family of semiaquatic bugs. The genus was described by Carpenter (1892), who coined the name from the Greek ~ p p u , a reef and /?uzqa, one who treads. The genus was originally placed in the Gerridae, but since the work of Poisson (1965), there has been general agreement that Hermatobates should be placed in a distinct family (Andersen & Polhemus, 1976; Andersen, 1982). The insects have generally been considered to be extremely rare: Herring (1965) noted that in two and a half years of entomological work in the South Pacific he had been able to collect only three specimens. There are at present nine species names, but the taxonomy of the Hermatobates species is in chaos. Our knowledge of the biology of the family is extremely limited. Cheng (1977) summarizes the existing sparse literature on the family and adds some useful observations of her own. The insects apparently live in crevices in coral rubble and boulders, emerging on to the water surface at low tide and retreating to their crevices as the tide returns. However, we still know almost nothing about the detailed distribution, zonation, development, or behaviour of Hermatobates.
In 1986 as part of the Pacific Phase of Operation Raleigh, I visited a number of Pacific islands and the present paper reports quantitative observations on the biology of this unusual family of intertidal animals.
MATERIAL AND METHODS
Systematics
The only reliable character for distinguishing the species of Hermatobates appears to be the structure of the male metasternum (Andersen, personal communication). Male specimens that I collected from Tonga and Fiji have been identified by Andersen as Hermatobates weddi China. The morphometry of the specimens from Samoa (Table 1) and the Cook Islands (not shown) is extremely similar to that of those from Fiji (Table l ) , but in the absence of adult males from these localities, I will refer to them as the Samoan and the Cook Island species, respectively.
Study sites
Observations and collections were made at 12 localities on nine separate islands (Fig. 1A). All but two of these localities were visited in 1986 as part of the
BIOLOGY OF HERMA TOBATES
A
89
- I n o
W. SAMOA
AM ERI cpi N SAMOA
. .*'TONGA
7 ..
I I1800 I 170°
Figure 1. A, Location of sites visited in the South Pacific; B, detailed map of study sites at Apia, Western Samoa (main islands of W. Samoa shown in inset). Stippling represents mangroves; dotted lines show outer margin of fringing coral reef.
Pacific Phase of Operation Raleigh. The other two sites, at Suva, Viti Levu and Tubou, Lakeba, were visited on an earlier expedition to Fiji in 1983 (see Foster & Treherne, 1986). The main study site was at Vaiala Beach, Apia, Upolu, Western Samoa, a coral rubble shore protected behind a fringing reef (Fig. IB).
Methods To sample the insects on the stones on the shore, individual stones were
immersed in seawater in a large washing-up bowl, and any insects that floated to the surf-ace whilst the stone was shaken around were collected. In zonation
90 W. A. FOSTER
studies, at each zone all the stones on the surface of the shore from five 50 x 50 cm quadrats were sampled by immersion in water. Any cavity larger than about 3 mm in diameter was defined as a ‘hole’.
In the transplant experiments, 15 suitable stones (i.e. with > 5 air-filled holes on the undersurface) were selected from the Hermatobates zone at Vaiala Beach and labelled with a red plastic ribbon. Five stones were then moved 5 m either along, up or down the beach. Four days later, the stones were sampled for the presence of live or dead Hermatobates In measurements of activity in relation to the tide, strips (2 m long and 1 m out to sea) of water adjacent to the shore were scanned for insects at regular intervals. With careful scrutiny, even the smallest instars could be seen on the water surface.
Biometrical measurements were made with a micrometer eyepiece on a Wild Stereomicroscope. Head width was measured across the dorsal surface of the head including the two compound eyes at the widest point. Legs were measured along the longest (dorsal) length of each segment. The small separate pieces between the antenna1 segments were not included in the measurements of the antennae.
In submergence experiments, the insects were placed individually in small lengths of plastic tube with nylon gauze over one end. The insects floated up against the gauze and their movements could be seen through a microscope. A continuous recirculated flow of seawater at 2 1-23°C was maintained over the containers in which the insects were held. The insects were inspected regularly and any that failed to respond to a prod were removed and observed to see if they recovered. The experiments were carried out on board the R.V. Sir Walter Raleigh.
Specimens used in microscopy had all been fixed in the field as whole animals in 70% alcohol. For scanning electron microscopy, the specimens were critical- point dried from absolute alcohol, mounted on universal aluminium stubs with carbon cement, sputter-coated with approximately 40 nm of gold in a Polaron Sputter Coater, and examined in a Philips SEM505. Scanning electron micrographs were also taken of 0.5 pm sections, embedded in Araldite, mounted on coverslips, and prepared as above, but without critical-point drying. For measurement of hair lengths, pieces of cuticle were fractured and viewed parallel to the plane of the cuticle. For light-microscopical examination of the eyes, 0.5 pm sections embedded in Araldite were stained with Methylene Blue.
RESULTS
Biometry and instar determination Analysis of population samples from Samoa and Fiji indicates that there are
four larval instars (Table 1; Fig. 2). The largest larval instar is definitely the final larval instar, since several of the specimens had soft adult cuticle visible under the larval cuticle. The smallest specimens are almost certainly the first instars. The smallest embryos and larvae measured by Andersen (personal communication) from Phuket Island, Thailand and from Onrust Island, Djakarta, had head widths of 0.56 mm. The prolarva figured in Andersen (1982; fig. 12) had a head width of 0.42 mm: however, it is well known that newly hatched larvae expand after eclosion by swallowing air.
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92 W. A. FOSTER
Head width (mm)
6.0 F B
5 3.0t - t‘ + z Fiji
Adults
0.5 0.6 0.7 0.8 0.9 1.0 1.2 1.4 1.6
Head width (mm) Figure 2. Morphometry of life-history stages of Hermafobah. Log length of hind leg (femur+tibia+ tarsus) against log head width (measured across the compound eyes). A, Specimens from Apia, Samoa. August 1986. The IV instars included six females and three males. Slope of the regression = 1.1 1 (1.06-1.15, 95% confidence interval); B, specimens from Fiji (Vuda, Suva, Lakeba). July 1983, August 1986. Slope of regression for 1-111 instars= 1.00 (0.81-1.19, 95% C.I.); for female IV instars and adults=1.23 (1.05-1.42, 95% C.I.); and for male IV instars and adults=2.11 (1.9e2.32, 95% C.I.). Slopes for 1-111 instars and females not significantly different; slope for males highly significantly different from slopes for both females and 1-111 instars (Gabriel’s approximate method: Sokal & Rohlf, 1981).
The instars can be distinguished on the basis of any of the morphological characters given in Table 1: the lengths of the mid or hind femora are probably the easiest to measure. There is a slight overlap in some of the characters of the largest fourth instar males and the smallest adult females: however, adults are clearly distinguishable by their three-segmented tarsi and the Y-shaped dorsal thoracic suture in the females and the prominent genitalia in the males. The gender of the fourth instars can be determined by the wider, stouter fore-femora of the males and the distinctive pattern of the abdominal sterna of the sexes. In the males, the last abdominal sternite is a broad plate, but in females it consists of two narrow plates that meet in the mid-line.
For the first three instars and the female fourth instars and adults, the relationship between head width and the length of the appendages is
BIOLOGY OF HERMATOBA7ES 93
approximately isometric (Fig. 2A); for Samoan specimens, the slope of the regression of the length of the hind leg on head width (log-log scales) was 1.1 1 (1.06-1.15; 95% C.I., Fig.2A) and 1.11 (1.07-1.16) for the middle leg on head width. However, for males (fourth instars and adults) the slope of these relationships was very much greater: for example, for Fijian specimens (Fig. ZB), the regression of length of hind leg on head width (log-log scales) was 2.1 1 ( 1.90- 2.32; 95% C.I.), for the middle leg on head width 2.09 (1.81-2.37), and for the antenna (segments 2, 3 and 4) on head width 1.70 (1.40-2.00) Because of this markedly allometric relationship, the males have a much greater range in appendage length than do the females for an equivalent range in head width (Fig. 2B). For example, in the Fijian specimens the longest mid leg in a male was 36% longer than the shortest (4.35-5.92 mm), whereas in the females, the range was only 11% (3.71-4.12 mm).
Anatomy
Eyes The eyes of Hermatobates (Samoan specimens: 2nd and 4th instars) have a
small number (30-40) of relatively large facets (c. 30-40 pm in diameter). The visual field, obtained both from histological sections and also by rotating intact preserved specimens in a goniometer, ranged between 145" and 1556. The interommatidial angles, estimated by dividing the total visual field by the number of facets (minus one) in the row, were between 18" and 25".
Despite the poor quality of the histology (performed on specimens preserved in the field in 70% alcohol) it is clear that the eye is basically of the apposition type with ommatidia isolated from each other by a pigment screen. In common with other semiaquatic bugs (Gerromorpha), e.g. Gerris (Langer & Schneider, 1970), there is an open rhabdom arrangement whereby the individual rhabdomeres of the retinula cells (at least seven in number) are not fused and are thus in principle capable of resolving the image. By analogy with Gerris and with the Diptera, one might expect that this situation would be exploited to enhance sensitivity using the mechanism of neural superposition (cf. Hardie, 1986), but detailed neuroanatomical tracing methods would be required to substantiate this. The relatively large facets, combined with the large interommatidial angles (c. Z O O ) , indicate that the eye would have a relatively high sensitivity but a low resolving power (an f number of c. 1-45).
Cuticular hair layers The body surface is clothed in long and short hairs. The long hairs occur on
almost the whole body surface including the appendages and between the lenses of the compound eyes: the hairs are between 40 and 90pm long, they taper gently to a point, are longitudinally grooved, and occur at densities of between 2500-6800 mm-*. The highest densities were found on the ventral abdominal surface of the adults. The micro-hairs have a distinctive rounded tip (Fig. 3). They form a dense layer, which in the adults covers the whole of the head, thorax and abdomen (but excludes the compound eyes or any of the appendages). In the juveniles, the micro-hair layer is more restricted: it covers the head and the dorsal surface of the thorax, stopping abruptly in a line across the first abdominal tergite just posterior to the first abdominal spiracle, and
94 W. A. FOSTER
Figure 3. Details of the hair-layers on the cuticle of Hcrmatobates. A, Ventral abdomen; B, C, dorsal prothorax; D, cuticle close to a metathoracic spiracle; E, cuticle around 2nd abdominal spiracle; F, dorsal surface of 1st abdominal tergite, showing abrupt discontinuity of the layer of micro-hairs. A is from an adult male H. lucddi (Tonga); B F , 2nd instar Hermatobates sp. from W. Samoa. Scale bars: A, E, F=lOpm; B, C, D = l p m .
BIOLOGY OF HERMA TOBATES 95
there are no micro-hairs on the ventral surface of the thorax and abdomen, although the layer does extend down the pleura of the thorax and abdomen to include the cuticle around the thoracic and abdominal spiracles (Fig. 4). This pattern of micro-hair covering corresponds precisely to the pattern of silvery air- layers seen when juveniles and adults are submerged in sea water.
The micro-hairs vary greatly in size. The smallest are stalkless blobs, less than 0.4pm long and 0.3pm in diameter. The longest, which occur around
abdominal spiracles
A
mesothoracic spiracle
met’othorocic spiracle
I mm
- ‘ P m
Figure 4. A, Distribution of cuticular hairs on an immature (2nd instar) H . weddz from Tonga. Antennae and legs have been removed. Scale bar= 1 mm; B, details of the hair layers on the dorsal metathorax. Length of the macro-hairs c. 60pm. Scale bar= 1 pm.
96 W. A. FOSTER
intersegmental membranes and the openings to the thoracic spiracles, are about 2.5pm long. In some hairs, the rounded tip is a little wider than the shaft, but typically the tip is a sphere two to three times wider than the end of the tapering shaft to which it is attached (Fig. 3). In any particular area the longest micro- hairs are of roughly uniform length, presenting a level layer of micro-spheres at the surface of the cuticle (Fig. 3). In many areas of the cuticle, there are two distinct types of micro-hairs: longer hairs with wide tips and an understorey of shorter hairs with smaller tips (Fig. 5). The distinction is not always as clear-cut as in Fig. 5, but in most areas of the cuticle where micro-hairs occur, there are distinct long and short hairs (see Fig. 3). The longer micro-hairs make up between 55 to 90% (mean 75%, 23 observations on seven immatures) of the total micro-hair count. The density of the micro-hairs ranges between 1.8 and 3 . 5 8 ~ 1O6rnmv2 on immatures (mean 2.46k0.13 (S.E.); 23 counts on seven insects from Samoa) and between 2.8 and 3.2 x lo6 mm-* on the ventral surface of the abdomen of adults (three specimens of H. weddi from Tonga). The tips of the larger micro-hairs are about 0.56 pm wide and the percentage area occupied by the tips of the larger micro-hairs when viewed from directly above was on average 30% (range 27-35y0, 15 measurements on the ventral thorax of three adult H. weddi from Tonga). The larger micro-hairs are arranged in a fairly regular array, although in some parts of some specimens they were somewhat clumped. The largest diameter circle that could be fitted between the larger micro-hairs, without touching them, was about 0.66 pm (ventral abdominal surface of Tongan adult). In some regions of the cuticle, for example in parts of the abdominal pleura, there are stout (about 0.6 pm at base), long (c. 2 pm) and pointed micro-hairs.
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0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8
Hair length (pin)
Figure 5. Dimensions of micro-hairs on the prothorax of an adult male H . weddi (Tonga). The total length of the hair, including the swollen tip, was measured. Measurements were taken on fractured pieces of cuticle, viewed at right angles to the hair layer in the SEM. Frequency distribution of the hairs of different lengths is given at the bottom of the figure.
BIOLOGY OF HERMATOBA TES 97
Does the micro-hair layer connect up with the spiracles so that any air trapped there could be used in respiration? The abdominal spiracles, in both juveniles and adults, are on raised protuberances and do not make connection with the layer of micro-hairs (Fig. 3F). However, the micro-hair layer does connect up with the mesothoracic and metathoracic spiracles. SEM photographs show that the entrance to these spiracles is surrounded by a dense layer of long (c. 2.5 pm) micro-hairs (Fig. 6). Light microscope sections show that these longer hairs occur at the entrance to the spiracle and could provide continuity between an air layer under the micro-hairs of the general body and the tracheal system via the thoracic spiracles (Fig. 6). The maximum path length for gases to travel from the air layer to a spiracle would be about 1.3 mm, the distance from the dorsal tip of the abdomen to the metathoracic spiracle in adults. In juveniles, which have no micro-hair layer on the abdomen (or on the ventral thorax), the maximum distance would be about 0.75 mm.
Submergence experiments
When submerged in recirculated sea water at 20-22"C, 50% of the immature Hermatobates (Samoan specimens) survived for about 11-13 h (Fig. 7). They
Figure 6. Scanning electron micrograph of a 0.5 pm section through the mesothoracic spiracle of an adult male Hcmtobates from Tonga: s-spiracle; sa-spiracular atrium. Arrows indicate the micro- hair layer. Note that the spherical tips of many of the micro-hairs (e.g. in bottom left of figure) have been broken off in the embedding medium. Scalebar= 10 pm.
98 W. A. FOSTER
0 4 8 12 16 20 24
Time (h) Figure 7. Survival of immature Hermatobafes: from Western Samoa when submerged in recirculated seawater at 21-23°C: --H- 20 insects, 4.8.86; --0- 30 insects, 6.8.86.
showed a variable response to submergence: most of the individuals remained active for at least 4 h, but after that time some became quiescent and those that did recover took between 3 and 30 min to regain activity when returned to air.
Distribution In the South Pacijic
Specimens of Hermatobates were found on all four of the island groups visited: in the Cook Islands on Rarotonga (Muri Lagoon and the shore near the airport); in the Samoas on Upolu, Western Samoa (Apia), and on Tutuila, American Samoa (Leone); in Tonga on Nukualofa (Tongatapu); and in Fiji on Viti Levu (Suva and Vuda Point) and Lakeba (Tubou) (Fig. 1 .) No specimens were found on three of the small islands of the Southern Cooks (Atiu, Mitiaro, Mauke).
On all the shores visited, juvenile Hermatobates were found only on shores strewn with coral rock, rubble and boulders. They were never seen in association with mangroves. Adults and final instar larvae were seen on the surface of the sea at distances of up to about 5 m from shore, for example around the edge of the fringing reefs at Vuda (Fiji) and around the piers and wharfs of Nukualofa harbour, Tongatapu (Tonga). The narrow fringing reefs of Atiu, Mitiaro and Mauke (Cook Islands) are very exposed and have no suitable rocks and boulders.
Local distribution At low tide, Hermatobates were found under stones in a narrow ( c . 20 cm)
vertical zone roughly centred around MLWN (Fig. 8). A similar distribution was found at both sites in Apia. The insects were only found in holes on the
BIOLOGY OF HERMATOBATES
2 1.4
E, 1.2 - 1.0
0.0 6 0.6 2 0.4 n
0.2 .P 0
-0.2
+
c .c
I
0 5 10 15 20 Distance (m)
Figure 8. Zonation of Hermatobates at Vaiala, Apia, W. Samoa, 2.8.86. At each sampling site, mean density ( & S.E.) was estimated from the numbers under stones in five 50 x 50 cm quadrats. Bar on right indicates the Hermatobates distribution in relation to height above Chart Datum. Waves indicate height of low tide on 2.8.86 (0.1 m above C.D.).
3 - b Q 2 b 6- E 2 -
5
r
f 4- n
z -
99
9/11 c-
undersurfaces of stones. Stones with less than five holes on the undersurface were not observed to harbour Hermatobates, and there was a general trend for an increase in insect numbers with an increase in the number of holes per stone (Fig. 9). The insects were highly aggregated. Sampling of 168 randomly selected
0
2- 12/26 -
0/26 0/31
100 W. A. FOSTER
stones within the Hermatobates ‘zone’ revealed 192 insects: 104 of these were under one stone and 147 of the stones contained no insects. The distribution of the insects per stone was very significantly non-random ( X = 1.14, s.d = 8.3, n = 168; tested against expected Poisson distribution, considering the number of rocks with 0, 1 ,2 ,3 or > 3 insects, G = 125, d.f.=P<c0.001). Stones that were partially buried in the substrate did not contain any Hermatobates.
An excellent method of assessing a stone’s suitability for Hermatobates is to turn the stone over whilst it is submerged at high tide. Only those stones that release air-bubbles when turned over ever contain any insects, which can clearly be seen floating to the surface. On 2.8.86, of 50 stones turned over at high tide in the Hermatobates zone that released air bubbles, eight contained some insects; whereas no insects were released from any of the 50 stones from the same zone that failed to release air bubbles. This is a good demonstration that the vital resource for Hermatobates on the shore is the space provided by cavities that remain air-filled at high tide.
Transplant experiments In an attempt to understand the factors determining the zonation of
Hermatobates, rocks from the Hermatobates zone that were considered to be suitable for the insects (see Methods) were moved 5 m either along, up or down the shore. The rocks were sampled four days later (Table2). The insects were unable to survive outside their usual zone, suggesting that they are absent from these higher and lower zones not because they cannot reach the areas or because suitable stones are unavailable, but because the conditions there are hostile to them.
Distribution of life-history stages The distribution of the different life-history stages from several locations is
given in Table3. On these sampling occasions, most of the insects collected under stones were young immatures (about 2% were adults and only 7% were final instars (n= 166)). In contrast, the insects collected from the water surface included a much higher proportion of adults and final instars: 79% adults and 15% last instars (n=71). The younger immatures did venture on the water surface (see Fig. lo), but they always remained very close to the shore amongst the lapping waves and were very difficult to collect. Although these samples (Table 3) were taken at a similar time of the year, they were taken in a range of localities and differences in instar distribution may merely reflect geographical differences in the timing of the life-cycle.
Activity during the tidal cycle
Hermatobates were only seen on the water in any numbers at low tide, although adults and final instars were observed at high tide at night at Nukualofa, Tonga (Table 3). Typically, the insects emerge from under the rocks as the tide ebbs past them, swim on the water surface near the water’s edge (although the adults and older instars may range further), and retreat back under the rocks after the tide has turned. This pattern was observed in all the localities visited, and Fig. 10 shows quantitative observations in Western Samoa and Fiji. The peak period of activity on the water surface is just before low tide.
BIOLOGY O F HERMATOBATES
TABLE 2. Transplant experiments at Vaiala, Apia, W. Samoa, 3-7.8.86. Values are mean number of alive and dead insects ( f S.E.) under five stones that, four days earlier, had been transplanted from the Hermatobates ‘zone’ 5 m either up, along or down the
beach
101
Mean number alive Mean number dead Treatment ( fS.E. , n = 5 ) ( fS.E. , n = 5 )
Up shore 0 0.2f0.2 Along shore 4.7f2. I 0 Down shore 0 1.0k0.5
Observations on feeding, moulting and mating Adults and juveniles were observed feeding on recently dead adult chironomid
midges (Clunio pacijicus Edwards and Tanytarsus halophilae Edwards) at low tide at Vuda, Fiji on 18.8.86. No other feeding records were obtained. Moulted cuticles, of all instars, were frequently found in the rock crevices (see Table3), and it seems clear that the insects moult in these dry air-filled spaces.
Copulation was observed twice in one pool at Vuda, Fiji at low tide on 19.9.86. There were about seven adults in the pool. In both cases, copulation began when the male climbed on to the back of the female whilst both were on the water surface. The pair then swam swiftly to the edge of the pool, where they climbed a few millimetres above the water surface and remained in genital contact on the coral for about three minutes. The pair then separated and the female swam off out of sight.
TABLE 3. The instar distribution of Hennatobates species collected from localities in the South Pacific. Only collections in which an attempt was made to capture all the Hennatobates in a particular patch
of habitat are shown
Adult Live or
Place Date Tide Position cast skins I I1 111 IV Female Male
Apia, Samoa
Apia, Samoa
Rarotonga, Cook Islands Vuda, Fiji
Suva, Fiji
Nukualofa, Tonga Nukualofa, Tonga
2.8.86 Low
4-7.8.86 Low
4.7.86 Low
19.8.86 Low
9.7.83 Low
12.8.86 High
12.8.86 Low (Night)
Under a single stone Under stones
Under stones
Water surface7 Water surface7 Water surface7 Under stones
Live Cast skins Live Cast skins Live Cast skins Live
Live
Live
Live Cast skins
3 5 3 3 4 4 1 0 2 1 3 2 0 0 0
35 26 18 4 0 0 8 1 5 1 0 0 0 1 3 0 2 0 0 1 1 0 0 0 0 0 2 2 1 7 * 5 *
0 0 0 5 23* 10*
0 0 0 5 4 7
0 2 3 2 2 1 1 1 0 0 0 0
~
7Insects caught more than 1 m from shore. *Including one pair in copula.
I02 W. A. FOSTER
I
- 0-m-
- 6.0
- 5.0 I
.- ._ ii - 4.0 NE
B
-3.0 p 2
- N
a
8
f - 2.0 $
- 1.0
- 0
I I 1 I I I -3 -2 -I Low tide +I t2 +3
Time ( h )
Figure 10. Numbers of Hematobales on the water surface in relation to the tidal cycle. - 0 - Vaiala, Apia, W. Samoa, 5.8.86; all immature insects. - ~~ Vuda, Fiji, 19.9.86: adults and immatures. Mean values kS.E. of counts on 25 (Samoa) or 15 (Fiji) 2 x 1 m strips of water surface adjacent to the shore.
DISCUSSION
The present observations provide the first detailed account of the resource requirements and vertical zonation of the Hermatobatidae. In general, Cheng's (1977) opinion that the insects are confined to coral rubble and reefs is confirmed. The essential requirement for Hermatobates appears to be rocks with cavities that remain air-filled at high tide. Rocks with crevices only on the upper surface, or with holes that are filled with sand because the rock is partially buried, or with holes filled with water because the rock is too low in the intertidal zone are not colonized by the insects. The zone of suitable habitats is restricted to a narrow (c. 20 cm) vertical band centred around MLWN (Fig. 8). The transplant experiments show that the insects are unable to survive outside this zone, presumably because there are no air-filled cavities lower in the intertidal zone, and perhaps because it is too hot and dry higher on the shore.
Hermatobates have a clearly defined tidal activity pattern: they emerge from their rocky crevices about an hour before low tide, swim on the water surface close to the shore during the low tide period, and return to their crevices by about an hour after low tide (Fig. 10). This is consistent with the qualitative observations made by Cheng (1977) and earlier workers (Walker, 1893; Esaki, 1947). I t is possible that some of the insects do not return to the rock crevices before high tide: a small number of adults and late instars were observed at high
BIOLOGY OF HERMA TOBATES 103
tide at night in Nukualofa, Tonga (Table3). However, the first three instars were never seen on the water surface at more than 1 m from the shore (Table 3). Adults and late instar nymphs have been recorded in small numbers on open water (Cheng & Leis, 1980; Cheng & Schmidt, 1982), but these have usually been regarded as strays.
I t has been suggested that Hermatobates are primarily nocturnal (Usinger & Herring, 1957), but the evidence is thin. Plankton tows for Hermatobates in open water have been more successful at night than during the day: 93% (n=44) and 69% (n= 13) of the netted specimens were collected at night, respectively in Hawaii (Cheng & Leis, 1980) and at Lizard Island on the Great Barrier Reef (Cheng & Schmidt, 1982). However, open water is probably not the typical habitat of the genus, and the low tide excursions, which clearly are characteristic of Hermatobates, certainly can occur during the day (Fig. 10). I t is not clear whether these low tide activities also occur at night. The eye of Hermatobates might well be adapted for night-time vision. The eye parameter (P) (facet diameter x interommatidial angle in radians), which is a valuable indicator of the visual environment for which an animal is adapted (Snyder, 1977; Snyder, Stavenga & Laughlin, 1977), has a value of 10-15pm in Hermatobates. This suggests that the insect is adapted to low levels of luminance, but this could be either for activity at night or life in holes on the undersurface of rocks.
These observations provide the fullest available account of the post-embryonic development of Hermatobates. The instars can readily be distinguished on the basis of any of the morphological characters used in Table 1. I t seems that there are only four larval instars. This is unusual, since almost all the Heteroptera have five instars (e.g. Richards & Davies, 1977), although some other semi- aquatic bugs (e.g. species of Mesovelia and Microvelia) have only four larval instars.
Hermatobates appears to have two methods for solving the crucial problem of respiration during tidal submergence: compressible air-bubbles and an incompressible plastron. Both of these air-stores can act effectively as gills, provided they are surrounded by well-aerated medium, as will generally be the case in the turbulent waters of the rocky intertidal zone. All the evidence indicates that the insects are enclosed in air-bubbles at high tide: insects experimentally released from stones at high tide or when washed from stones at low tide always emerged with bubbles of air, completely dry and unwetted. I t is possible that the primary function of these air-filled crevices is not in aiding respiration but in providing a dry living space in which the insects can moult and move around freely during tidal submergence. The insects may identify suitable holes by the use of pheromones, since all stages, but especially the adults, give off odours that are readily detectable by humans.
The evidence that Hermatobates has a plastron is less clear-cut. Presumably, a plastron would only be required if for some reason the air-bubble around the insect collapsed or the insect chose an inappropriate hole in which to spend high tide. The micro-hair layer has most of the attributes of a plastron. The hair density (1.8-3.6 x lo6 mrn-') is almost as high as that recorded for Aphelocheirus (c . 4 x lo6 mrn-'; Hinton, 1976a, b), which is known to have a highly effective plastron (Thorpe & Crisp, 1947a, b). The shape of the micro-hairs-a vertical shaft, with a large swelling at the tip-is also analogous to the shape of the Aphelocheirus hairs, which are vertical with bent-over tips. In addition, the
104 W. A. FOSTER
relatively regular and uniform length of the longer micro-hairs in Hermatobates indicates that they could be effective at maintaining an air-water interface between each of the tips. By analogy with other plastron-bearing insects (e.g. Hinton, 1968, 1976a, b) the micro-hair layer of Hermatobates ought to be able to withstand the excess pressure provided at high tide: on the shores studied, the highest tides would be about 2 m (equivalent to 0.2 atmospheres). This could be tested directly with live specimens. During submergence, the pattern of silvering, which reveals the trapped air-layer in the micro-hairs, corresponded precisely to the pattern of distribution of the micro-hairs themselves, both in the juveniles and adults (Fig. 4). Most importantly, it has been shown that the air beneath the micro-hairs could connect with the tracheal system at the meso- and metathoracic spiracles (Fig. 6). In many insects, where micro-hair layers have been described as ‘plastrons’, no evidence has been provided that the supposed air-film connects with the spiracles (e.g. Aepophilus bonnairei (Signoret) (King & Ratcliffe, 1970); Halobates and Ventidius (Cheng, 1973)). However, if the micro- hair layer of Hermatobates does function as a plastron, it is surprising that the insects are not able to survive longer when submerged in aerated seawater (Fig. 7). Further experiments, involving measurements of oxygen consumption, are required.
The micro-hairs are unlike those of any other semiaquatic bug. The micrographs of Cheng (1977) do not reveal the swollen tips of the micro-hairs of Hermatobates: this may be because she was looking at a part of the cuticle where the tips are relatively small, or perhaps because the tips are absent in hairs of that particular species. The micro-hair layer of Hermatobates is closest in design to that of Halobates, which resembles an array of golf-clubs with the heads oriented in the same direction (Cheng, 1973; Andersen, 1977). Halobates, unlike Hermatobates, is not regularly submerged and would seem to have little use for a plastron for respiratory purposes. The function of the understorey of smaller micro-hairs in Hermatobates is unclear: possibly, as Andersen ( 1977) has suggested for the filamentous outgrowths at the base of the Halobates micro-hairs, they function to keep the longer micro-hairs apart and help the plastron withstand high pressures.
The present observations underline the point, already made by Cheng (1977), that this fascinating family of marine insects is not as rare or elusive as originally thought. Indeed, the Hermatobatidae are probably regular members of the fauna of rocky, coral shores throughout the tropics. Much remains to be learnt about them. In particular, it would be nice to obtain more precise information about their respiration and behaviour during submergence; to discover how they find their way back to suitable holes after low tide; to sort out their taxonomy; and to provide field data on how they feed, copulate and lay their eggs.
ACKNOWLEDGEMENTS
This research was carried out as part of the Pacific Phase of Operation Raleigh (OR). I am indebted to the directing staff of OR, the crew of the RV Sir Walter Raleigh, the headquarters staff-especially Eibleis Fanning and Nicholas Payne-and the Venturers, in particular those who helped me in the Treaders project-Jayne Ayers, Phil Moran, Maggie Fraulo, Lee Hastie and Matthew Richmond. I would like to thank Nils Meller Andersen for his help and good
BIOLOGY O F H E R M A T O B A I E S 105
advice; Maggie Bray and Mick Day for their patient and invaluable work in preparing the electron micrographs; and John Rodford for assistance in preparing the figures. I am grateful to Roger Hardie and Helen Skaer for their helpful comments. The work was supported by a Travelling Fellowship from the British Ecological Society and by a travel grant from the University of Cambridge.
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