J. Zool., Lond. (1987) 211,357-372

Reproductive biology of the intertidal spider Desis marina (Araneae: Desidae) on a New Zealand rocky shore

C. L. MCLAY AND T. L . HAYWARD Department of Zoology, University of Canterbury, Christchurch, New Zealand

(Accepted 29 May 1986)

(With 1 plate and 4 figures in the text)

Desis marina is an intertidal spider which lives within rock crevices and cavities in the holdfasts of the brown kelp Durvillaea antarctica, where it is submerged in the sea for long periods. Spiders live within silk-lined retreats which enclose an air bubble, and mate location is restricted to periods when the nest is exposed to the air. Eggs are laid from September to January and emergence is complete by May, with the major recruitment period being from March to April. During June to August, females are reproductively inactive. Egg development requires two months and the first two instars remain in the nest for a further two months. Number of egg sacs laid is independent of female size but number of eggs per sac increases with size. Egg size and number of eggs per sac is independent of brood sequence. Female reproductive investment is only 17.6% of body weight, but with 3 to 4 egg sacs/female, nest-guarding time is in excess of five months. Females reproduce only once per year and may reproduce again in the following summer. Desk marina has a much lower clutch size than comparable terrestrial spiders and is a ‘bet-hedger’, producing sequential broods which spread recruitment over time and reduce the risk of total loss due to storms.

Contents

Introduction . . . . . . . . Methods . . . . . . . . . .

Development terminology Results . . . . . . . . . . . .

Nests and broods . . . . Reproductive season . . Fecundity . . . . . . . . Nest-guarding . . . . . .

Discussion . . . . . . . . . . References . . . . . . . . . .

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Introduction

Desis marina (Hector, 1877) lives along the shoreline of New Zealand and some of its off- shore islands (Stewart and Chatham Islands). The distribution of the 14 species in this genus has been discussed by Roth & Brown (1976) who show that Desk is a widespread Indo-Pacific genus. Most species seem to live at a lower level in the intertidal zone than any other maritime spiders. Besides D . marina, the only other member of this genus to have received attention is D . formida- bilis from South Africa. How these spiders manage to survive in this alien environment has been studied by Lamoral (1968a, b, 1971), McQueen & McLay (1983) and McQueen, Pannell & McLay

0022-5460/87/002357 + 16 $03.00 @ 1987 The Zoological Society of London 357

358 C . L . M c L A Y A N D T . L . H A Y W A R D

(1983). Water relations and haemolymph composition have been investigated by Moloney & Nicolson (1984) and population ecology and habitat use by McLay & Hayward (In press). As yet, no studies have been made of the reproductive biology of any of the Desis species.

We decided to undertake a study of the reproduction of D. marina to enable us to make comparisons with the already extensive studies that have been made of the reproduction of terrestrial spiders (Enders, 1976). The aim of our study was to ascertain the reproductive season, fecundity/size relationship and brood nest structure of this spider.

Desis marina is an ecribellate spider which does not construct a web or snare but lives in a simple retreat or nest which is built within the tunnels of the brown alga Durvillaea antarctica, or on some shores in rock crevices or under limpet shells. In these shelters, spiders gain protection from the waves and also find a moist micro-habitat which protects them against desiccation. The nest is only large enough to accommodate one spider (or two spiders in cohabiting pairs) and it must also completely enclose the brood. Since spiders must often withstand long periods (2-3 weeks) of submergence under the sea, they must be extremely efficient users of oxygen and ensure that their nest volume is sufficiently large (McQueen & McLay, 1983). This places severe restrictions on the number of spiders which can live together and restricts the period of mate- location to occasions when the nests are exposed to the air (McLay & Hayward, In press).

Our study of Desis marina population structure (McLay & Hayward, In press) showed a female-biased sex ratio, 1.36 females/male, with females growing to a larger size than males. Recruitment to the population peaked in February and May (late summer and autumn) but at no time were there large numbers of juveniles. Solitary spiders were most commonly encountered, but most of the population lived with conspecifics. When males and females were found in the same kelp holdfast they cohabited (occupied the same nest). Most females were found alone in winter but pairing-up occurred in the spring (from September onwards), and mating could potentially occur in most months except late winter. Some females may survive to breed again in the following year, but males probably only have one breeding season. Male and female size of cohabiting pairs was positively correlated, suggesting that mating occurs between similar-sized spiders. The average Dyar’s constant was 17.2%, with no relationship between adult moult increment and pre-moult size and no difference between male and female increments. The results presented here complement those of our earlier paper.

Methods

Our study area was at Kean Point, Kaikoura (42’25”35’S, 173’43”15’E) on a coastline that is very exposed to wave action. A more detailed description of the area can be found in McQueen & McLay (1983) and McLay & Hayward (In press). In this area, Desis marina occupies kelp holdfasts (Durvillaea antarctica), living in the cavities created by burrowing and grazing animals such as limpets and chitons.

Collection of spiders was carried out at approximately monthly intervals, from December 1981 to February 1983, during spring tides when the holdfasts were fully exposed to the air. In total, 2655 holdfasts were examined and we aimed to collect at least 30-40 spiders per month. We found that 14.5% of holdfasts contained at least one spider and that distribution of spiders on the shore was extremely patchy. A detailed description of the collection methods can be found in McLay & Hayward (In press). The data which we collected consisted of: spider size (carapace length and total length), sex, number per nest, number per holdfast, presence or absence of broods and area of the holdfast. All broods collected were opened and examined. The number of eggs and first and second instars per egg sac was recorded. The terminology used is as follows: brood chamber (or brood) refers to a silk sac which consists of between 1 and 5 individual egg sacs and thus contains the female’s total reproductive output for a given period of time; clutch is used

REPRODUCTIVE BIOLOGY O F D E S I S M A R I N A 359

synonymously with egg sac and refers to a cluster of eggs oviposited at one time, which are enclosed in a silk pouch. The individual egg sacs of one female are woven together to form a brood. Nest silk and brood chamber silk were examined under a Cambridge Stereoscan 600 scanning electron microscope. Material was air-dried and then mounted on stubs and coated with 50 nm of gold.

Development terminology Eclosion and late embryonic development of spiders have been studied by Holm (1940, 1954) and Vachon

(1957, 1958, 1965). These 2 authors proposed quite different nomenclatures for the stages of development. Eclosion is not a simple ‘before’ and ‘after’ event and there is no general agreement on the point at which this term should be applied. In this paper, the rupture and sloughing of the external egg membrane will be considered as eclosion (i.e. the point of hatching), even though in D . marina and some other spiders the emerging spider is still enclosed in a second inner egg membrane. Chorion and vitelline membrane refer to the outer and inner egg membranes, respectively (Johannsen 8z Butt, 1941). A more serious problem lies in the terminology for the spider itself just before and after eclosion. Because it is clearly defined and to some extent established in araneological literature, the terminology proposed by Vachon (1 957) is probably the most useful. However, in order to be consistent with most recent works written in English (e.g. Peck & Whitcomb, 1970), the following terms will be used: first post-embryo (Vachon’s second pre-larva) will designate the period immediately following eclosion in which the spider is still enveloped in the vitelline membrane; second post-embryo (Vachon’s larva) will designate the ambulatory stage that follows casting of the vitelline membrane. These 2 stages together will be considered as the first instar and the stage that follows the first true moult will be called the second instar. The first instar is probably best regarded as part of the embryonic stage.

When first laid, the eggs of D. marina are spherical, creamy white and nonagglutinate. As the embryo develops, the egg becomes more ovoid and the contours of the embryo, especially those of the appendages, are imprinted upon the chorion. The chorion then ruptures (eclosion) revealing the first post-embryo still enclosed by the vitelline membrane. The second post-embryo which emerges from the vitelline membrane is a small (1.9-2 mm total length) white spider with unsegmented legs, no hairs, eyes or fangs. Although active, movements of the legs are unsteady. During this stage, pigments begin to collect and form eye spots and darkened patches at the tips bf the chelicerae in preparation for the fangs. There is no evident growth between the second post-embryo and second instar (i.e. following the first moult). However, the second instar emerges from the exuviae as a radically transformed animal. The legs and palps now show distinct segmentation and the fangs are developed and folded back on to the medial face of the chelicerae. The claws are developed and the combs on the claws are evident. The abdomen and legs are densely covered with grey hairs and spines are also present. After a period in the egg sac, the second instars emerge into the female’s nest. Emerged juveniles are referred to as spiderlings. According to Vachon’s nomenclature, the pattern of development of D. marina is (pL1, pLZ)L(PN)+Nymphs+Adult, where pL1 is the first pre- larva, pLz is the second pre-larva, L is the larva, PN is the pre-nymph and Nymphs are the juvenile stages up to the mature Adult. Spiders were not considered to be part of the population until they had emerged from the egg sac.

Results

Nests and broods Nests are located along the under-surface of the holdfasts so that at least one side of the nest

opens into the interior of the holdfast. The exact shape of the nest is largely determined by the shape of the tunnel within which it is built. The nest volume is entirely enclosed by a silk sheet which, following disturbance, the spider can break open, by tearing and biting at the silk using

360 C. L. M c L A Y A N D T . L . H A Y W A R D

PLATE I. (a) Scanning electron microscope photo of nest silk of Dais marina. Two thicknesses of silk are used, c.1.54 pm and 0.38 pm diameter. (b) Scanning electron microscope photo of brood silk. The wall is multi-layered strands of silk c. 1.5 pm diameter.

REPRODUCTIVE BIOLOGY OF DESZS M A R I N A 36 1

its chelicerae. Of all the 385 nests examined, only one was found that was not built against the holdfast surface; in this case an empty limpet shell attached to the holdfast had been used. On very sheltered shores, we have recorded D. marina under limpet shells lying among rocks.

Desis marina can spin a nest in a relatively short time. A flimsy, transparent nest which encloses the spider can be constructed in c. 2 min. These nests are waterproof, trapping a bubble of air when submerged. The nest is constructed of two different thicknesses of silk. First, thicker strands (1.54 pm diam.) are laid at approximately right angles to each other to form a base structure (see Plate Ia). These strands are laid down such that strands running in one direction are woven over and under the strands running in the other direction. Secondly, a lace-work of thinner (0-38 pm diam.) strands is laid on top of the thick strands, forming a mat of silk and completing the nest wall. In the laboratory, spiders were observed to continue adding silk to the inside of the nest while under water so that the walls became thicker, white in colour and no longer transparent. In this manner, the nest becomes strong and durable to the movement of water in and out of the holdfast.

The brood chamber is lenticular in shape and is made of strong, closely woven silk which has a distinct pinkish hue. The brood consists of from one to five individually woven egg sacs which are strongly stuck together. However, each egg sac can be separated without damaging the contacting walls. The brood chamber is woven from evenly sized strands of silk which are the same diameter as the thicker strands (c.1-54 pm diam.) used in the nest (see Plate Ib). These strands are laid randomly in all directions and often double back on themselves. In cross-sections, the brood chamber is made up of many layers in a mesh-like fashion with very fine silk threads connecting the layers.

Reproductive season Females with broods (eggs and/or first and second post-embryos) were found in all months

except June, July and August, while females with spiderlings in their nests were found in each month. The average percentage of females with eggs was 12-3%, with the highest recorded in April (33%), and the highest level of spiderlings was recorded in May (Fig. 1). The sequence of

100

80

D J F M A M J J A S O N D J F Month

FIG. 1. Percentage of Desis marina females (n = 240) with broods (0) and spiderlings (0) in their nests at Kaikoura from December 1981 to February 1983.

362 C. L. McLAY A N D T. L. HAYWARD

TABLE I Summary of occurrence of nest-bound oflspring of h i s marina at Kaikoura. Figures in brackets are percentages

No. Months nests Eggs PEl PE2 I2 Total

Dec. '81 1 77(68.8) 10 (8.9) 10 (8.9) 15(13.4) 112 Jan. '82 2 136(67.3) 7 (3.5) 59(29.2) 0 202 Feb. 5 159(32.3) 58(11.8) 107(21.8) 168(34.1) 492 Mar. 1 4 l(28.3) 9 (6.2) 0 95(65.5) 145 April 2 0 0 0 54( 100) 54 May 2 0 0 0 46(100) 46 June 0 0 0 0 0 0 July 0 0 0 0 0 0 Aug. 0 0 0 0 0 0

Nov. 1 43(100) 0 0 0 43

Sept. 1 50(100) 0 0 0 50 Oct. 1 17(100) 0 0 0 17

DW. 3 136(100) 0 0 0 136 Jan. '83 4 312(88.6) 0 0 40( 1 1.4) 352 Feb. 4 140(32.9) 17 (4.0) 107(25.1) 162(38) 426 Totals 27 llll(53.5) lOl(4.9) 283(13.6) 580(28.0) 2075

Dec. '81 -Nov. '82 523(45.1) 84(7.2) 176( 15.2) 378(32.5) 1161 Jan. '82-Dec. '82 582(49.1) 74(6.2) 166( 14.1) 363(30.6) 1185 Feb. '82-Jan. '83 758(56.8) 67(5.0) 107 (8.0) 403(30.2) 1335 Mar. '82-Feb. '83 739(46.1) 84(5.2) 214(13.4) 565(35.3) 1602

Totals 2602(49.3) 309(5.8) 663(12.5) 1709(32.4) 5283

__

development begins in September (spring) when the first eggs are laid (Table I), and hatching does not begin until December when the first post-embryos and second instars appear in the population. Post-embryo stages are present until March, and during the December-March period, second instars increase in relative abundance until, by April, all eggs have hatched and only second instars are found in the broods. By June, all second instars have emerged from the brood sacs. During June to August (winter), adult spiders are reproductively inactive. There were some differences between summer 1981-82 and summer 1982-83. During the first summer, all four stages of brood development, from eggs to second instars, were present in December at the beginning of the study, but at the same time in summer 1982-83 only eggs were found. Second instars were found in January 1983 and all four stages were present in February. It seems likely that, by chance, our December 1982 sample did not pick up post-embryos and yet they must have been present to account for the presence of second instars in January 1983. Therefore, the reproductive pattern is probably egg laying from September to March and post-hatching brood development from December to May.

Field data suggest that egg development requires approximately two months (estimated from first eggs in mid-September to first hatchlings in mid-November) and post-hatching brood development also requires two months (estimated from last eggs at end of March to last hatchlings at end of May), which means that the total time spent in the brood sac would be four months. These estimates can be checked as follows: if we assume no mortality between stages of brood development then, given random sampling, the relative abundance of the four stages over a 12- month period will reflect the relative length of time spent in each stage. Given a 15-month study, four estimates of these relative abundances are possible (see Table I). The proportions of total

REPRODUCTIVE BIOLOGY OF DESZS M A R I N A 363

brood time spent in each stage are as follows: eggs (range 45.1-56.8, mean = 49.3%), first post- embryos (5.0-7.2, 5.8%), second post-embryos (8-0-15.2, 12.5%), second instars (30.2-35.3, 32.4%) and all post-hatching stages (43-1-54.9, 50.7%). These compare well with the develop- mental sequence observed: eggs (50%) and post-hatching (50%), i.e. two months each. Approxi- mate duration of post-hatching stages are: first post-embryos (0.23 month or 7 days), second post-embryo (0.50 month or 16 days) and second instar (1.3 months or 40 days). As a result of the assumption of no mortality between stages, it is to be expected that the proportion of time spent in the first post-embryo stage would be over-estimated and the proportion spent in the second instar would be under-estimated. However, even assuming that the 10% mortality during the egg stage (see below) continued for subsequent stages, the likely errors are small in relation to the errors resulting from monthly sampling. Our data indicate that D. marina offspring could spend about four months in the nest before dispersal.

Examination of the composition of individual brood sacs suggests that development within a clutch of eggs is fairly well synchronized. In most broods, all offspring were in the same stage of development or span two adjacent stages. Some cases showed clear evidence of non-development of eggs where all but a few had proceeded to an advanced stage. Egg mortality in these cases was on average 10.01 +4-5% (95% confidence interval, n = 9). Where several clutches are present, they were often at different stages of development, suggesting that they had been laid over a period of time. The mean interval between clutches is 14.8 f 2.8 days (95% confidence interval, n =49) or approximately two weeks. This was estimated from intervals between broods at different stages of development using the above estimates of duration of each stage.

These estimates of duration of each stage can be used to estimate the age of each clutch and then to produce expected egg laying and hatching dates for a 12-month period. These dates can be checked against the observed onset of egg laying and the last date of emergence of spiders from the nest. The agreement between observed and predicted dates is excellent, with egg laying expected to begin in early September and the last offspring emerging in late May (Fig. 1). Nest- bound offspring can be found for a total of 38 weeks and the non-breeding period is about 14 weeks and occurs in winter. Egg laying continued for approximately 20 weeks, as did emergence from the nest, and there was an overlap of only about 1-2 weeks between cessation of egg laying and onset of emergence. The majority of eggs were laid during late October-early December and the majority of young emerged from the nest during March-April (see Fig. 2).

Ottaway (1976) found that average sea temperatures in the Kaikoura study area during 1973-75 increased from 8 "C (July) to 18 "C (January) and decreased again. Egg laying by D. marina began in September when the sea temperature would be approximately 10 "C and continued until January when sea temperatures would have reached their maximum. The mean temperature during embryonic development would be 13 "C. Spiderlings did not emerge until December, when the temperature would be 15-16 "C and emergence continued until April, when temperatures had begun to decrease towards 13-14 "C. Sea temperatures during the non-reproductive period would have been 8-9.5 "C.

Fecundity Fecundity of females which had completed their egg laying increases with spider size (Fig. 3).

The number of egg sacs per female (mean = 3.4 +0.54,95% confidence interval) was independent of female size but number of eggs per sac increased with female size 0, = 3.34~-13.27, rz = 0.37, Pt0.001, d.f. = 69). Hence, total egg production per female also increased with female

364 C. L . McLAY A N D T . L. H A Y W A R D

2 4 6 8 10 12 14 16 18 20 22 24 26

Two-weekly period

FIG. 2. (a) Estimated percentage of eggs laid by Desis marina each two-weekly period at Kaikoura during a year. Open circles (O), based on field data from December 1981-November 1982; triangles (A), January 1982-December 1982; squares (m), February 1982-January 1983; closed circles (o), March 1982-February 1983. (b) Estimated percentage of spiders emerging from nests each two-weekly period. Symbols as for (a).

size (y = 13-56x-64-84, rz = 0.43, P = 0.004, d.f. = 15). Thus female fecundity ranged from 46 to 202 eggs per female (mean = 98.3f21-2, 95% confidence interval). Number of eggs per sac ranged from 11 to 61 (mean 27-6+_2.5,95% confidence interval). The order in which an egg sac was laid did not account for any of the variance of eggs per sac (Fig. 4). The mean number of eggs per sac remained essentially the same (range 28.68-24.5 eggs, mean = 27.6) but the variance of the early brood size was greater than for the later broods. Also, egg size was not related to egg sac order ( P > 0-05). Mean egg diameter was 1-13$_0.021 mm (n = 44) and mean egg volume was 0-77+0.43 mm3. Egg size was independent of female size (P > 0.05). Since a female builds only a single brood nest per summer and tends the eggs during their development, the average number of eggs laid per reproductive season is approximately 100. If only one repro- ductive season is completed successfully, then in a stationary population mortality must be around 98%.

Female investment in egg production (egg weight c. 0.1 mg) was independent of female size and averaged 17.6+2.9% (95% confidence interval, n = 17) of female body weight. The invest- ment per egg sac averaged 4-9&0-43% with an average maximum investment per sac of 6.1 f0.12%. Thus a female may invest 4.9% of her body weight every two weeks (interval between broods) when reproducing. It may be possible for a female to lay more than one egg sac at a time as some broods had more than one egg sac at a similar stage of development. However, since the ageing technique is very coarse the evidence for this is not conclusive.

REPRODUCTIVE BIOLOGY OF DESZS M A R I N A

. . . . - - - - _ _ _ _ _ _ _ _ . . . . . . . * Mean=3.4

365

I , I 1 I 9 10 11 12 13 14 15 16

180L 160

140-

120-.

[5) m al

!5 L2

z 5 100-

80-

I I I I 1 8 9 10 11 12 13 14 15 16

Total length (mm)

FIG. 3. (a) Relationship between number of egg sacs/female and female total length (mm) for Dais marina at Kaikoura. (b) Relationship between number of eggslsac (0). total number of eggs/female (0) and female total length (mm). Equations of regression lines given in the text.

Nest-guarding The majority (80%) of broods were accompanied by lone females with only two accompanied

by a male, two accompanied by another female and one by a large juvenile spider. The presence of the female appears to be essential for successful emergence of the young spiders, even though no females were seen to open an egg sac to allow spiderlings to emerge. Broods maintained in the laboratory without females did not hatch, while those with the female hatched normally. When the non-emerged broods were opened, they were found to contain well-developed second instars. The silk surrounding the brood is very tough and, although the young have small fangs, we assume that it is necessary for the female to tear open the sac and allow the spiderlings to emerge. In addition, the presence of the female is likely to be essential to maintain the integrity of the nest during the four-month development period. Following emergence, the young spiders may disperse to adjacent holdfasts or be carried away on the water.

366 C. L . M c L A Y A N D T. L. H A Y W A R D

4 0 1 0

0 00

a

1 2 3 4 5 6 Egg sac

FIG. 4. Relationship between number of eggs/sac and laying sequence for D a i s marina at Kaikoura. Closed circles (a)

indicate mean clutch size for each egg sac.

Discussion

There are two important features of the development of D . marina. First, there is a delay between shedding of the chorion and shedding the vitelline membrane. This is contrary to the general rule for spiders that both egg membranes are shed simultaneously (Holm, 1954; Vachon & Hubert, 1971). Secondly, D . marina moults only once inside the egg sac before emergence. Both of these features are true of Chiracanthium inclusum (Clubionidae) (Peck & Whitcomb, 1970) and Tetragnatha laboriosa (Tetragnathidae) (Le Sar & Unzicker, 1978). Vachon & Hubert (1971) found in three species of Agelenidae (Tegenaria saeva Bl., Coelotes terrestris Wid. and C. atropos Wlk.) that the vitelline membranes from the first and second pre-larvae are shed simultaneously with the chorion at eclosion. While D . marina and the Agelenidae differ in this respect, they are similar in having two pre-larva stages compared with only one in the Pholcidae, Dipluridae and Atypidae and none in the Theraphosidae. Desis marina does not exhibit the direct development from larva to nymph characteristic of the Agelenidae. Instead, like the Pholcidae, D . marina has an incomplete stage (the pre-nymph) following the larva.

Spider life cycles range from rapidly maturing species which can produce two generations per year up to long-lived species which require ten years to reach maturity. However, most spiders maintain a more or less annual cycle (Levy, 1970). Males and females usually take a similar length of time to reach maturity, but the life span of females is often somewhat longer than for males (Levy, 1970, table 111). Levy has classified spiders into two life cycle groups and Desis marina seems to belong to the first of the groups, which includes spiders in which mates derive from cocoons laid about the same time. Within this group, D . marina would belong to the second group of Bonnet (1935) where eggs are laid in spring or summer, spiderlings attain an immature stage, overwinter and reach maturity in the next spring or summer. But if D . marina females do indeed survive to lay eggs in the following summer, then it is possible that they will mate with

REPRODUCTIVE BIOLOGY OF DESZS M A R I N A 361

males that developed from eggs laid in the preceding season. Indeed, it is possible (although very unlikely given wide dispersal) that they could mate with their own sons.

Desis marina probably has a similar life cycle to the well-known water spider Argyroneta aquatica (Agelenidae). Bristowe (1958) recorded that males of this species mated with females in their nest in the spring and females laid up to three egg sacs during the summer each with 50-100 eggs. Eggs hatched in 3-4 weeks and the young spiders bit their way out of the brood sac, remaining with the female for a further 2-4 weeks before departing to build their own retreats or dispersing aerially on threads of silk. Argyroneta aquatica is the freshwater equivalent of D. marina in that it traps a source of prey unavailable to terrestrial spiders. Mostly, males and females are 9-13 mm TL but the occurrence of large females up to 28 mm TL suggests that they may be longer lived than D. marina females and may reproduce in more than one successive summer.

The only comparative reproductive data for other Desis species are those of Hickman (1949). Desis kenyonae from Tasmania (approximately the same latitude as our study area) seems to repro- duce at about the same time as D. marina. Hickman (1949) found two egg sacs on 4 December 1947: one sac contained 30 eggs and the other contained 30 second instars almost ready to emerge. The egg sacs were made of white silk with a tough, parchment-like outer layer and were accompanied by the female spider (unfortunately, female size is not given). A female kept in the laboratory laid eggs which hatched 47 days later. Newly hatched young remained in the sac and after 14 days 'underwent their first post-embryonic ecdysis'. We assume that this refers to the moult to the second instar. Further development was not recorded. These data suggest that D . kenyonae probably has a similar period of egg development to D . marina (two months), assuming that rate of development was enhanced by higher laboratory temperatures. The same applies with the moult to the second instar which occurs after about 23 (7 + 16) days in D. marina. Females of both species guard their broods and the clutch size of 30 recorded for D. kenyonae is very close to that of a D. marina female of 12-5 mm TL.

In the field, Desis marina spends about four months in the nest prior to dispersal as spiderlings. Egg development requires about two months and the early stages remain in the nest for a further two months, when sea temperatures average 13 "C. Phidippus johnsoni also spends equal amounts of time in egg development and early stages, although the total amount of time in the nest is only six weeks at 23-25 "C (Jackson, 1978). The total amount of time in the nest for other spiders is also much less than D. marina: Tarentula kochi (development temperature 15 "C, Hagstrum, 1970), Geolycosa godeflroyi (approximately 25 "C, Humphreys, 1976), Latrodectes hasselti (27-29 "C, Cariaso, 1967), one month, Oxyopes scalaris (approximately 22 "C, Cutler, Jennings & Moody, 1977), Argiope argentata, A . aemula (approximately 25 "C, Robinson & Robinson, 1978), three weeks and Metaphidippus galathea (27 "C, Horner & Starks, 1972), Lyssomanes viridis (temper- ature not given, Richman & Whitcomb, 1981) only one week. The long egg development period and nest-bound period of D . marina is probably attributable to the low environmental temper- atures. Since this spider spends much of its time submerged, it is rarely exposed to the higher temperatures experienced by terrestrial spiders. This long developmental period, coupled with sequential egg laying, requires a long period of nest-guarding by the female of the order of five months.

Desis marina females produce a similar number of egg sacs (mean = 3.4) regardless of body size, but eggslsac increase with size so that total fecundity increases with female size. However, female investment in egg production (weight of eggs as a percentage of body weight) is independent of female size. This averaged 17.6% for total fecundity and investment per egg sac averaged 4.9%. Hagstrum (1970) provides comparative data on female investment: Tarentula kochi (40%, one egg

368 C . L. M c L A Y A N D T . L. H A Y W A R D

sac), Gnaphosidae (3479, Thomisidae (134%), Theridiidae (46%) and Amaurobiidae (35%). Data from Edgar (1971) show 115% for the first egg sac and 79% for the second egg sac of Pardosa lugubris, with 194% investment for a 17 mg female completing two egg sacs. These data suggest that female investment by D . marina is considerably lower than for other spiders. This is the result of both small clutch size and small egg size.

Successive egg sacs laid by D a i s marina contained a similar number of eggs (mean 27.5) and the coefficient of variation decreased from 45% for the first sac to 17% for the fifth sac. The typical pattern established for other spiders is for later egg sacs to contain fewer eggs (Bristowe, 1958; Cazier & Mortenson, 1962; Mikulska & Jacunski, 1968; Edgar, 1971; Jackson, 1978). Also, the proportion of eggs which hatch decreases in later sacs (Jackson, 1978). In estimating the emergence patterns of D . marina spiderlings, no allowance was made for the possibility that later egg sacs contained fewer fertile eggs. Decrease in egg numbers with successive sacs has been attributed to sperm depletion and seasonal changes in prey availability. Neither of these factors seem to be important for D . marina which cohabits with males in most months and lives in a habitat where prey availability is unlikely to vary widely during the breeding season.

Egg size was not related to either female size or order of the egg sac laid by Desis marina. Edgar (1971) found that eggs in the first (summer) egg sac laid by Pardosa lugubris were lighter (0-53 mg/egg) than eggs in the second (autumn) egg sac (0.64 mg/egg). Heavier autumn eggs may enhance survival of spiderlings over the winter. Turnbull (1962) found that the egg weight of Linyphia triangularis was influenced by food supply ranging from 0.13 mg/egg (low food) to 0.37 mg/egg (high food). However, number of eggs/female was not affected by food supply over the range investigated (0-135-0-75 mg dry weight/day). Hence, L. triangularis females on low food supply packed a smaller amount of material into the same number of eggs. These results suggest that spiders can vary their packaging of material which provides the sole source of energy for the embryo (which in the case of L . triangularis develops over the winter), but it is likely that survival of spiderlings from small eggs may be reduced. Presumably, the trade-off between egg size and egg number has been optimized to produce the greatest number of surviving offspring. Desis marina does not vary either number of eggs/sac or egg size between broods. Larger females put more eggs in each sac but they do not invest any greater proportion of their body weight in eggs than do smaller females.

Data on clutch size in relation to female size shows a strong positive relationship with a marked difference between different spider families (Petersen, 1950; Enders, 1976). The relationship for D. marina ( y = 3.34~-13.28) is most similar to non-web building species of the family Clubionidae ( y = 5 . 1 8 ~ - 2.5) and web-building species of the family Agelenidae ( y = 12.98x-44.2), which are regarded by Roth (1967) as being closely related to the Desidae. However, the major difference lies in the extremely low clutch size of D . marina. Average clutch size for a 15 mm TL female would be: 37 for D . marina, 75 for Clubionidae, 150 for Agelenidae and 129 for all spiders (see Table 11, Enders, 1976). Enders observed that decreasing slope of the regression equation was associated with an increasing degree of activity during foraging. Further, that species with small clutches have a lower net income (capture rate) of prey. On both of these patterns, D. marina would seem to be exceptional. It lives in a habitat where its prey (amphipod and isopod crustaceans) are super- abundant and it spends a large portion of its time encapsulated in the nest. It appears to be a ‘sit- and-wait’ predator, capturing prey from its immediate surroundings. Only rarely are spiders seen moving over the intertidal rocks or plants. It may be that feeding opportunities for D . marina are severely restricted by the small size of the nest on whose surface prey may be captured, and by their confinement to the nest which results from submersion in the sea. Thus, while prey may be very

REPRODUCTIVE BIOLOGY OF D E S I S M A R I N A

TABLE I1 Some reproductive characters of spiders

369

Egg diam. No.

Species Eggslsac (mm) sacs Total eggs Source

Metaphidippus galathea (Salticidae)

Pardosa lugubris (Lycosidae)

Philodromus praelustris (Thomisidae)

Desis marina (Desidae) Pardosa californica

(Lycosidae) Linyphia triangularis

(Linyphiidae) Pardosa uintana

(Lycosidae) Lyssomanes viridis

(Salticidae) Tetragnatha laboriosa

(Tetragnathidae) Pardosa mackenziana

(Lycosidae) Pardosa concinna

(Lycosidae) Tarentula kochi

(Lycosidae) Phidippus johnsoni

(Salticidae) Oxyopes scalaris

(Oxyopidae) Tegenaria atrica

(Agelenidae) Diguetia canities

(Diguetidae) Pardosa tristis

(Lycosidae) Lutrodectus harselti

(Theridiidae) Geolycosa godeffroyi

(Lycosidae)

19

21-34.9

25.3

27.6 29

32

37.5

42.7

53

57.5

59.4

60

67.1

71

75.9

113

1 15.9

234

335

0.8 1

2-2.1 * -

1.13 1.9*

1.56*

-

1 .O

0.55

-

-

2.3*

-

0.8

1.2

0.77

~

0.22

2.4*

8.3

2

7.3

3.4 1

I?

1

1

2

1

1

1

3.1

-

9.5

4

1

11.7

1.8

158

57.9

185

98.3 29

32

37.5

42.7

106

57.5

59.4

60

207.9

-

721.4

480

115.9

2737

603

Homer & Starks

Edgar (1 97 I )

Putman (1967)

This study. Hagstrum (1970)

Turnbull (1 962)

Schmoller (1970)

Richman & Whitcomb

LeSar & Unzicker

Schmoller (1970)

Schmoller (1970)

Hagstrum(l970)

Jackson (1978)

Cutler, Jennings & Moody (1977)

Mikulska & Jacunski (1 968)

Cazier & Mortensen (1962)

Schmoller (1970)

Cariaso (1967)

Humphreys (1976)

(1972)

(1981)

(1978)

* Diameter estimated from egg weight assuming spherical shape and the same den- sity as D. marina (0.13 mg/mm3)

abundant, the spiders may still live a low prey-income habitat due to restricted opportunities for foraging.

An alternative explanation of low clutch size for D . marina may be that each offspring must be equipped with a comparatively large energy store to supply its needs during the long nest-bound period (four months), and that as a result fewer eggs can be laid. Unfortunately, there are very few comparative data on spider egg sizes in the literature, although we anticipate that the usual trade- off between egg-size and egg numbers that is seen in many other animal groups will probably also be found among spiders (see Hagstrum, 1970 for some data). There is only a limited amount of energy available for reproduction and this may be dispensed in many small ‘parcels’ or a few large

370 C. L. McLAY A N D T . L . HAYWARD

‘parcels’, according to the needs of the offspring. The hypothesis that D. marina packs its repro- ductive energy into a small number of large units cannot at present be tested.

AD. marina female literally does put all her eggs in one ‘basket’, i.e. nest. What can be the point of this when the eggs are laid at different times (iteroparic) and yet they are all in the same nest? Why doesn’t she put each sac of eggs in a different nest? The first problem is that her presence is required for successful hatching of young and she cannot be in more than one place at a time. Therefore, she keeps all the eggs together. This must imply that the probability of losing the whole reproductive output by demise of the nest is very small. So why not just lay one large egg sac? There are probably limitations on how much energy she can store up and put into eggs at any one time, but there may also be some value in spreading out egg laying and having offspring hatch at different times. The main hazard faced by offspring dispersing passively on the surface of the sea is the effect of storms which would probably cause high mortality of spiderlings. Therefore, the advantage of laying several sequential egg sacs may be to spread the risk of dispersal failure by the young. In this way, D. marinamay be a ‘bet-hedger’ in the sense of Stearns (1976). Such an hypothesis is supported by the fact that D. marina has a low reproductive investment and lays a similar number of eggs of the same size in each egg sac. Clutch size may be explained by Lack’s hypothesis (1954) that females produce, on average, the most productive clutch size which is set by the amount of food that females can capture and store up, given that each egg must be provided with sufficient material to meet the needs of the young spider.

A survey of the recent literature on spider egg laying in relation to egg size is shown in Table 11. In addition, Richter, Hollander & Vlijm (1971) show that Pardosapullata and P.prativaga produce similar numbers of eggs per sac to the Pardosa spp. in Table 11, but some may produce a second egg sac. Almost 50% of the species are semelparous, reproducing only once. Probably very few females of these species survive to reproduce in the following year. The remaining species are iteroparous either by producing several egg sacs in the same season or they reproduce again in the following year. Iteroparous species produce from 1.8 to 11.7 egg sacs/female/year. Desis marina may be iteroparous in both senses, producing several egg sacs in successive seasons. It has one of the lowest number of eggslsac but multiple laying places it at the median in overall fecundity. In terms of egg size, D. marina is again at about the median for this selection of spiders. Its eggs are not especially large compared to other spiders and thus requiring a trade-off with clutch size. The data in Table I1 show that egg diameter is only significantly negatively correlated with number of sacs, i.e. species

TABLE I11 Spearman’s Rank Correlation Coeficients between brood

characteristics for species listed in Table II

Egg Number Total Eggslsac diam. (mm) of sacs eggs

Eggslsac 1 .o -0.11 0.07 0.57 ** NS NS Egg &am. (mm) 1 .o -0.56 -044 * NS Number of sacs 1.0 0.71 *** Total eggs 1 .o

NS = not significant at 0.05; * = P < 0.05; ** = P < 0.01; *** = P < 0.001

REPRODUCTIVE BIOLOGY O F DESZS M A R I N A 37 1

which lay small eggs tend to have large numbers of sacs (Table 111). Hence semelparous species tend to put more into each egg than iteroparous species. But egg size is not correlated with clutch size or total number of eggs laid. Not surprisingly, eggs/sac and number of sacs are significantly positively correlated with total number of eggs.

We are pleased to acknowledge the assistance of Lindsay Smith, Philippa Gordon, Tracey Osborne, Don and Winnie McQueen and Simon Pollard with the collection of spiders on the shore. Jack van Berkel also provided valuable assistance at the Edward Percival Field Station, Kaikoura. The figures were prepared by Clinton Duffy. We are indebted to Robert Jackson who suggested and encouraged us to undertake this study.

REFERENCES Bonnet, P. (1935). La longkvitk chez les Araignkes. Bull. SOC. ent. Fr. 4 0 272-211. Bristowe, W. S. (1958). The worldojspiders. London: Collins. Cariaso, B. L. (1967). Biology of the black widow spider Latrodectus hasselti Thorell (Araneida, Theridiidae). Philipp.

Cazier, M. A. & Mortenson, M. A. (1962). Analysis of the habitat, web design, cocoon and egg sacs of the tube weaving

Cutler, B., Jennings, D. T. & Moody, M. J. (1977). Biology and habits of the lynx spider Oxyopes scalaris Hentz

Edgar, W. D. (1971). Seasonal weight changes, age structure, natality and mortality in the wolf spider Pardosa lugubris

Enders, F. (1976). Clutch size related to hunting manner of spider species. Ann. ent. SOC. Am. 69(6): 991-998. Hagstrum, D. (1970). Ecological energetics of the spider Tarentula kochi (Araneae: Lycosidae). Ann. ent. SOC. Am. 63:

Hector, J. (1877). Note added to the paper by C. H. Robson entitled ‘Notes on a marine spider found at Cape Campbell’.

Hickman, U. V. (1949). Tasmanian littoral spiders with notes on their respiratory systems, habits and taxonomy. Pap.

Holm, A. (1940). Studien iiber die Entwicklung und Entwicklungsbiologie der Spinnen. Zool. Bidr. Upps. 1 9 1-214. Holm, A. (1954). Notes on the development of an orthognath spider Zschnothele karschi Bos & Lens. Zool. Bidr. Upps.

Homer, N. V. & Starks, K. J. (1972). Bionomics of the jumping spider Metaphidippus.galathea. Ann. ent. SOC. Am. 6 5

Humphreys, W. E. (1976). The population dynamics of an Australian wolf spider, Geolycosa godefioyi (L. Koch 1865)

Jackson, R. R. (1978). Life history of Phidippusjohnsoni (Araneae: Salticidae). J. Arachnol. 6 1-29. Johannsen, 0. A. & Butt, F. H. (1941). Embryology of insects and myriapods. London: McGraw-Hill. Lack, D. (1954). The natural regulation of animal numbers. Oxford: Clarendon Press. Lamoral, B. H. (19684). On the species of the genus Desis Walckenaer, 1837 (Araneae: Amaurobiidae) found on the

rocky shores of South Africa and South West Africa. Ann. Natal Mus. 2 0 139-150. Lamoral, B. H. (1968b). On the ecology and habitat adaptations of two intertidal spiders, Desis formidabilis (O.P.

Cambridge) and Amuurobioides africanus Hewitt, at ‘The Island’ (Kommetjie, Cape Peninsula) with notes on the occurrence of two other spiders. Ann. Natal Mus. 2 0 151-193.

Agric. 51: 171-180.

spider Diguetia canities (McCook) (Araneae: Diguetidae). Bull. S. Calif. Acad. Sci. 61: 65-68.

(Araneae: Oxyopidae). Ent. News 88: 87-97.

Walck. in Central Scotland. Oikos 2 2 84-92.

1297-1 304.

Trans. Proc. N.Z. Znst. 10 299-300.

Proc. R. SOC. Tam. 1949 3 1-43.

30: 199-221.

602-607.

(Araneae: Lycosidae). J. Anim. Ecol. 4 5 59-80.

Lamoral, B. H. (1971). These spiders are drowned every day. Afr. wild Life 2 5 7-10. LeSar, C. D. & Unzicker, J. D. (1978). Life history, habits and prey preferences of Tetragnatha laboriosa (Araneae:

Levy, G. (1970). The life cycle of Thomisus onustus (Thomisidae: Araneae) and outlines for the classification of the life

McLay, C. L. & Hayward, T. L. (In press). Population structure and use of Durvillaea antarctica holdfasts by the

Tetragnathidae). Env. Ent. 7(6): 879-884.

histories of spiders. J. Zool., Lond. 160: 523-536.

intertidal spider Desis marina (Araneae: Desidae). N.Z. J. Zool.

372 C. L. McLAY A N D T . L. HAYWARD

McQueen, D. J. & McLay, C. L. (1983). How does the intertidal spider Desis marina (Hector) remain under water for

McQueen, D. J., Pannell, L. K. & McLay, C. L. (1983). Respiration rates for the intertidal spider Desis marina (Hector).

Mikulska, I. & Jacunski, L. (1968). Fecundity and reproduction activity of the spider Tegenaria atrica C. L. Koch. Zool.

Moloney, C. L. & Nicolson, S. W. (1984). Water relations and haemolymph composition of two intertidal spiders (Order

Ottaway, J. R. (1976). Inshore sea temperatures at Kaikoura, New Zealand, 1973-1975. Mauri Ora 4 69-73. Peck, W. B. & Whitcomb, W. H. (1970). Studies on the biology of a spider, Chiracanthium inclusum (Hentz). Bull. Ark.

Petersen, B. (1950). The relation between size of mother and number of eggs and young in some spiders and its

Putman, W. L. (1967). Life histories and habits of two species of Philodromus (Araneida: Thomisidae) in Ontario. Can.

Richman, D. B. & Whitcomb, W. H. (1981). The ontogeny of Lyssomanes viridis (Walckenaer) (Araneae: Salticidae) on

Richter, C. J. J., Hollander, J. den & Vlijm, L. (1971). Differences in breeding and mortality between Pardosa pullata

Robinson, B. & Robinson, M. H. (1978). Developmental studies of Argiope argentata (Fabricius) and Argiope aemula

Roth, V. D. (1967). Descriptions of the spider families Desidae and Argyronetidae. Am. Mus. Novit. No. 2292: 1-9. Roth, V. D. & Brown, W. L. (1976). A new genus of Mexican intertidal zone spider (Desidae) with biological and

Schmoller, R. (1970). Life histories of alpine tundra Arachnida in Colorado. Am. Midl. Nut. 83: 119-133. Stearns, S. C. (1976). Life-history tactics: a review of the ideas. Q. Rev. Biol. 51: 3-47. Turnbull, A. L. (1962). Quantitative studies of the food of Linyphia triangularis Clerck (Araneae: Lynyphiidae). Can.

Ent. 94: 1233-1249. Vachon, M. (1957). Contribution a l'ttude du dkveloppement postembryonnaire des araignkes. 1 . Gknkralitks et

nomenclature des stades. Bull. SOC. zool. Fr. 8 2 337-354. Vachon, M. (1958). Contribution B I'ttude du dkveloppement postembryounarie des araigukes. 2. Orthognathes. Bull.

SOC. zool. Fr. 83: 429-461. Vachon, M. (1965). Contribution l'ttude du dtveloppement postembryonnaire des araignkes. 3. Pholcus phalangioides

(Fuessl.) (Pholcidae). Bull. SOC. zool. Fr. 90: 607-620. Vachon, M. & Hubert, M. (1971). Contribution a I'ktude du dtveloppement postembryonnaire des araignkes. Bull. Mus.

natn. Hist. nut. Paris (Zool.) No. 11: 613-624.

such a long time? N.Z. J. Zool. 10: 383-392.

N.Z. J. Zool. 10: 393-400.

Pol. 1 8 97-106.

Araneae). J. exp. mar. Biol. Ecol. 83: 275-284.

agric. Exp. Stn No. 753: 1-76.

significance for the evolution of size. Experientia 6 96-98.

Ent. 99: 622-631.

Magnolia grandyora L. Psyche, Camb. 88: 127-133.

(Clerck) and Pardosaprativuga (L. Koch), (Lycosidae, Araneae) in relation to habitat. Oecologia 6 318-327.

(Walckenaer). Symp. zool. SOC. Lond. No. 42: 31-40.

behavioural notes. Am. Mur. Novit. No. 2568: 1-7.