The pattern of tube-sharing in Micro deutopus gryllotalpa (Crustacea: Amphipoda)

Anirn. Behav., 1980, 28, 790-797 THE PATTERN

OF TUBE-SHARING (CRUSTACEA:

IN MICRODEUTOPUS AMPHIPODA)

GR YLLOTALPA

Bv BETTY BOROWSKY*

Osborn Laboratories of Marine Sciences, New York Aquarium, New York Zoological Society, Boardwalk at W. 8th St., Brooklyn, N Y 11224 Abstract. The amphipod crustacean Microdeutopus gryllotalpa builds tubes on solid substrata. Mature animals usually reside in individual tubes. When more than one individual is present in a tube it is always a single heterogametic pair. Tube-sharing occurs with the greatest frequency 12 h before the female's moult. Following the female's moult, most males leave the tube. The pattern of tube-sharing is the behavioural analogue of precopulation in epibenthic amphipods. It is demonstrated that (1) no more than two individuals are found in a tube because (2) one individual will not permit another individual of the same sex to cohabit the same tube, and (3) the female determines the time of tubesharing, for most females tube-share only shortly before they moult. It is hypothesized that after the male leaves the female's tube, he cruises from tube to tube until he gains entry into the tube of another receptive female. Physiological constraints can influence patterns of behaviour in animals. In gammarid amphipod Crustacea ovulation only occurs shortly after the female moults (Kaestner 1970). Therefore, in non-sperm-storing species, copulation must occur close to the time of the female's moult. To ensure the presence of a male at this time, females of epibenthic gammarids permit a male to carry them about a few days prior to the moult (called precopulation). Shortly after the female's moult, copulation occurs, the pair separates, and ovulation follows. This precopulation behaviour guarantees the presence of viable eggs and sperm at the same time, ensuring fertilization. Precopulation behaviour has not been observed in several species of tube-building gammarids, however. Mature adults of Ampelisca vadorum and A. abdita leave their individual tubes in the substratum and swim freely in the water when the moon is full. Copulation probably occurs at that time (Mills 1967). This paper reports the existence, in Microdeutopus gryllotalpa, of another mechanism for satisfying the requirement of the presence of a male at the time the gammarid female is due to ovulate. Microdeutopus gryllotalpa builds its tubes on hard substrata along the North Atlantic coast (Bousfield 1973). Each individual constructs a tube around itself that is about the same diameter as its own cross-section. The tube is composed of sand, algae, and whatever debris is available, held together by threads spun by the animal. In the laboratory, tubes are built by adults o f both

Materials and Methods L Maintenance of Stock Cultures All animals tested were taken from stock cultures begun from animals collected from the low tide mark at Jamaica Bay, New York. Stock cultures were maintained in 19-cm glass culture dishes three-quarters filled with sea water adjusted to 24 ppt (the average salinity at the collecting site) and covered by glass plates. The water was taken from the collecting site, or prepared from Instant Ocean Sea Salts (Aquarium Systems, Eastlake, Ohio). Water was not aerated and was changed only if it became cloudy. Animals were supplied with chopped Ulva sp. thalli ad libitum. The Ulva were obtained from the intertidal zone at Jamaica Bay, frozen, and then defrosted and used as needed. The Ulva served both as food and tube-construction materials. Occasionally, bits of the ribbed mussel Modiolus demissus adductor were provided, since the animals appeared to be healthier when fed meat. Animals were maintained on a 12L: 12D cycle, at 20 C except where noted. Observations were always made during light periods.

*Present address: Department of Biology, 952 Brown Building, New York University, Washington Square, New York 10003.

H. Body Length Measurements Accurate body length measurements require that the animal, which is generally curled ven-

sexes, and by juveniles as early as one day after emergence from the marsupium. Preliminary observations and Myers (1971) suggested that adults of the same sex were never found in the same tube. Sometimes, however, tubes contained one male and one female. It is shown here that heterogametic tube-sharing occurs just prior to the female's moult.

790

BOROWSKY: TUBE-SHARING IN MICRODEUTOPUS GR YLLOTALPA trally while alive, be straightened out. Since straightening out the animals while holding them immobile generally injured them, the animals were first tested, then fixed in formalin, then straightened out and measured. The distance from the dorsal tip of the rostrum of the head to the posterior dorsal tip of the telson was measured in millimetres.

III. The Pattern of Tube-Sharing A. The spatial pattern of tube-sharing. The number and sex(es) of all mature individuals (over 3.0 mm in body length) were determined in two culture dishes. Further, for each individual it was noted (1) whether it was in or out of a tube, and (2) whether it was alone or sharing a tube with another individual. B. The temporal pattern of tube-sharing. Sixteen siblings, isolated shortly after emergence from the brood pouch and raised until either the mature brood pouch or male characters of the first gnathopods were observed, were employed for this experiment. Siblings were employed to reduce genetic variability. Four heterogametic pairs were placed, one pair per dish, in culture dishes for 14 days. Abundant building materials were provided. On the 15th day, the pairs were rearranged: two females were placed in one, and two males in another, clean dish. Abundant building materials were again supplied. Thus, during the first 14 days each animal was a member of a heterogametic pair, and during the next 14 days each animal was a member of a homogametic pair. Four other pairs were arranged as homogametic pairs for the first 14 days and as heterogametic pairs for the next 14 days. Animals were maintained at room temperatures (~ ---- 22.2 C q- 1.7). The light cycle, 15L:9D, was chosen to simulate the L:D cycle in the field during the animals' reproductive season. The light period was 0600 to 2200 hours. I observed the dishes every 12 h (at 0700 hours and 1900 h o u r s ) a n d noted whether the animals occupied the same tube or not, plus any signs of reproductive activity. C. The pattern of distribution after the female ovulates. Thirty dishes, each containing one tubesharing pair, were stripped of all materials other than the tubes and the animals inside them. Within 24 h after the female's moult, (1) the number of occupants and (2) the sex(es) of the occupant(s) in the tube were noted. IV. The Mechanism of Tube-Sharing A. General methods. The objectives of these experiments were to determine: (1) why three or

791

more mature animals were never found in the same tube; and (2) how the animals determined the time of tube-sharing. Animals that had recently been tube-sharing were arranged in heterogametic pairs. Each pair was placed in a 10.5-cm culture dish. An animal that was introduced into a dish containing a single tube attempted to enter it, even if it was already occupied. At that time, interactions between the introduced animal and the original occupant(s) of the tube could be observed under the microscope. B. Interactions between individuals not sharing tubes. One hundred and twenty heterogametic pairs that were not tube-sharing were arranged in three experimental groups of 40 pairs. Within each experimental group, 20 tests were conducted, each using two pairs. In the first experimental group, both males were switched between dishes. In the second experimental group, the females were switched. In the third experimental group the male of one dish and the female of the other dish were switched. Thus, observations were made on four test situations: (1) a male introduced into a female's dish; (2) a female introduced into a male's dish; (3) a male introduced into a male's dish; and (4) a female introduced into a female's dish. The following were observed: (1) the occurrence o f tube-sharing versus contests; (2) the final occupant(s) of the tube (if any); (3) the relative sizes o f the combatants; and (4) the relative size of the winner, if any. An interaction between two individuals was scored as a contest when either (1) only one individual was the final occupant; or (2) no individuals remained in the tube. A 'winner' of a contest was defined as the final occupant of the tube. Interactions generally lasted about 10 s. An observation was terminated and scored as a contest when either one or both individuals were entirely Outside of the tube. An observation was terminated and scored as tube-sharing when one individual's head was facing one of the open ends of the tube and the other individual's head was facing the other end.

Results I. The Pattern of Tube-Sharing in Mass Culture A. The spatial pattern of tube-sharing. Most individuals were alone in individual tubes (Table I). Seven of 107 tubes contained two individuals, and these were all heterogametic pairs. No tube contained either homogametic pairs or more than two mature individuals. There were significantly more males than females found outside

792

ANIMAL

BEHAVIOUR,

tubes although there were more females than males in the dishes (Z21 = 13.10, P < 0.01). B. The temporal pattern of tube-sharing. O f 216 observations of eight homogametic pairs, the two animals were never in the same tube. O f 220 observations of eight heterogametic pairs, the two animals were in the same tube 108 times. In all the heterogametic pairs there were times when the pair shared the same tube and times when they were in different tubes. Twelve hours before a female's cast, or moulted exoskeleton, was first observed, the pair was in the same tube significantly more often than expected (16 tube-sharings versus 2 nontube-sharings, ~21 = 10.92, P < 0.01). Twelve hours before a male cast was observed, there was no significant difference between the number of times the pair shared a tube (3) and the number of times they were in separate tubes (6; Binomial Test, P > 0.05). Further, there was no significant difference between the number of times the pair shared the same tube and the number o f times they did not 12 h after the female moult (7 and 12 respectively; X2I = 0.70, P > 0.05) and 12 h after the male moult (3 and 5 respectively; Binomial Test, P > 0.05). Thus, although tubesharing was not confined to times immediately prior to the female's moult, most females did share tubes at that time. Precopulation behaviour was never observed either inside or outside a tube. Copulation was observed three times, and it occurred within the tube each time. C. The pattern of distribution after the female moults. Males were larger in 12 pairs, females were larger in 12 pairs, and both animals were the same size in 3 pairs. Twenty-four hours after the female's moult, pairs were separate significantly more often than they were together in the tube (28 versus 2 times; ~21 = 22.53, P < 0.01). When one individual was outside and one inside the tube, males were outside significantly more often than females (23 versus 4; ;~21 ---- 13.37,

28,

3

P < 0.01). Both individuals remained inside the tube twice and both individuals were outside the tube once. Thus 24 h after the female moulted and ovulated, the pair usually separated, and usually only the male left the tube. II. The Mechanism of Tube-Sharing A. Interactions between pairs not sharing tubes. (la) Homogametie tests, females introduced to females' tubes. Although introduced females attempted to enter the original occupant's tube in each of the 30 tests, no tube-sharing ever resulted. Larger females were the final occupants significantly more often than were smaller females (24 versus 6 times; Z21 = 10.80, P < 0.01). Introduced females won more often than the original occupants, but the difference was not significant (20 versus 10 times; Z21 = 3.33, P > 0.05). Both size and which animal was introduced determined which animal won a contest. O f the 16 larger females introduced 15 were the final occupants, but of the 14 smaller females introduced only 5 were winners (Binomial Test, P < 0.01 and P > 0.05, respectively). (lb) Homogametie tests, males introduced to males' tubes. Introduced males attempted to enter the original occupants' tube in only 26 of 30 tests. In the remaining four tests introduced males spent some time at the entrance of the tube but did not attempt to enter it. No tube-sharing resulted. Winners were larger significantly more often than they were smaller (19 versus 7; X21 = 5.54, P < 0.05). Further, introduced males were winners significantly more often than were the original occupants (20 versus 6; Z21 = 7.54, P < 0.01). Of the 13 larger males introduced, 13 were winners, but of the 13 smaller males introduced, only 7 were winners (Binomial Test, P < 0.01 and P > 0.05, respectively). Thus, both size and which animal was introduced influenced which animal won a contest. (2a) Heterogametie tests, males introduced to females' tubes, Males attempted to enter females'

Table I. Spatial Distribution of All Individuals over 3.0 nun in Two Culture Dishes (107 Occupied Tubes)

Outside tubes

Inside tubes Inside tubes Sharing tubes as member as member with two or of a of a more Inside tubes heterogametie homog.ametic mature alone parr pair individuals Totals

Number of males

9

30

7

0

0

46

Number of females

1

70

7

0

0

78

BOROWSKY: TUBE-SHARING IN MICRO DEUTOPUS GRYLLOTALPA tubes in every test. Tube-sharing resulted 7 of 30 times; the male was larger once and the female six times (Binomial Test, two-tailed, P > 0.05). Males were larger in 9 and females in 13 contests, and they were the same size in one. Larger individuals, regardless of sex, won significantly more often than did smaller individuals (Zel = 6.26, P < 0.01; Table IIA). Introduced males won more often than the occupant females, but the difference was not significant (;~el = 2.13, P > 0.05; Table IIA). (2b) Heterogametie tests, females introduced to males' tubes. Females attempted to enter males' tubes in every test, and tube-sharing resuited 14 times. The male was larger four times, the female was larger nine times, and they were of equal size once (~21 = 1.92, P > 0.05). There was no significant difference between the number of times larger and smaller individuals, regardless of sex, won contests (Binomial Test, P > 0.05; Table liB). However, the original occupants, the males, won significantly more often than did the females (Binomial Test, P < 0.01 ; Table IIB). (2c) Heterogametic tests, differences between the introduction of a male and the introduction of a female when tube-sharings result. The occurrence of tube-sharing instead of a heterogametic contest was not associated with the relative sizes of the two individuals (sections 2a and 2b above), Table II. Characteristics of Final Occupants after Heterogametic Contests between Currently Non-Tube-Sharing Individuals A. Males Introduced to Females' Tubes

Sex Size Number larger Number smaller Totals

Number males

Number f e m a l e s Totals

9.5 5.5

8 0

17.5 5.5

15.0

8

23.0

but with which sex was introduced. The number of tube-sharings that resulted when a female was introduced to a male's tube (14 of 30 tests) was significantly greater than the number that resuited when a male was introduced to a female's tube (7 of 30 tests) (Z2t : 4.09, P < 0.05). Thus, even though neither individual had been tubesharing before the test, males were more likely than females to permit the opposite sex to enter their tubes and remain inside. (2d) Heterogametie tests, differences between the introduction of a male and the introduction of a female when contests result. In those tests in which contests rather than tube-sharings resuited, sex, not size, was important in determining the winner when females were introduced (occupant males won more often), but size and sex were important in determining the winner when males were introduced (introduced males and larger animals won more often). Males won heterogametic contests more often than females (section IIA2 above). B. Interactions between individuals sharing tubes. (1) General results. None of the 60 tests resulted in more than two individuals sharing a tube, and the two final occupants were always a heterogametic pair. However, the final occupants were often not the original pair. When an introduced animal attempted to enter a tube, a contest occurred significantly more often than not (Z21 : 20.83, P < 0.01; Table III). The number of homogametic contests was significantly greater than the number o f heterogametic contests (~z 1 = 15.0, P < 0.01, Table III). The winners of Table HI. Sex(es) of Combatants in Contests that Occur after One Currently Tube-Sharing Individual is Introduced to a Tube Containing a Tube-Sharing Pair Female introduced

Number of:

19

Number of: Sex

Number larger Number smaller Totals

Number males

Female-female Male-female No contests c o n t e s t s contests 9

2

Male introduced

B. Females Introduced to Males' Tubes

Size

793

Number f e m a l e s Totals

Male-male Male-female No contests c o n t e s t s contests 26

1

3

Heterogametic contests

No contests

7 7

2 0

9 7

Homogametic contests

14

2

16

45

Totals:

10

5

794

ANIMAL

BEHAVIOUR,

homogamefic contests were usually larger than their opponents (32 o f 42 contests; Z21 = 11.52, P < 0.01), but there w a s n o significant difference between the number of original occupants and introduced animals that won (18 and 24, respectively; Z 2 1 = 0.86, P > 0.05). Generally, when a pair shared a tube, the male's antennae projected from one end, and the female's antennae projected from the other. Thus, it was expected that an introduced animal would be equally as likely to encounter a male as a female at the end of the tube that it attempted to enter. However, the number of times a male was encountered by an entering animal was significantly greater than the number of times a female was encountered (Z21 = 10.28, P < 0.01; Table IV). This was because males often moved to the end the introduced animal was entering. (2) M a l e s introduced, Homogametic contests occurred significantly more often than heterogametic contests (26 versus 1; Z21 ~ 23.14, P < 0.01). Larger males won more often than did smaller males but the difference was not significant (17 versus 8; Z21 = 3.24, P > 0.05). There was no significant difference between the number of original occupants and the number o f introduced males that won (14 versus 12; Z21 -----0.15, P > 0.05). Table IV. Number of Times Each Member of a TubeSharing Pair was Encountered by an Introduced Individual that had Just Been Tube-Sharing

Not observed

Male and female Female at same encounend tered

Male encountered

Female introduced

1

1

8

20

Male introduced

2

0

8

20 "

Totals

3

1

16

40

28,

3

(3) F e m a l e s introduced. Table V shows that when contests resulted, and the original occupants were at opposite ends of the tube, femalefemale contests resulted every time the introduced females attempted e n t r y at the females' end, whereas male-female contests resulted only half the time when females entered the males' ends. The difference is significant (Fisher E x a c t Probability Test P = 0.02). When a female entered at the male's end, either a contest resulted, or the male moved over and permitted the female to enter. I f the female entered, when she encountered the occupant female, a contest resulted. Males won all heterogametic contests. In the 18 homogamefic female contests in which one female was larger than the other, larger individuals won significantly more often than did smaller ones (16 versus 2; ~21 = 10.89, P < 0.01), but there was no significant difference between the number of occupants and the number of introduced animals who won (12 versus 14; Z21 = 0.15, P > 0.05). C. T h e b e h a v i o u r o f individuals sharing tubes versus individuals n o t s h a r i n g tubes. The number

of times a female permitted a male to enter the tube was significantly greater when both animals were currently tube-sharing (but with different partners) than when both animals were not tubesharing (Fisher Exact Probability Test, P < 0.01). However, males accepted females with equal probability whether or not they were currenfly tube-sharing ( ~ 2 1 = 0.55, P > 0.05; Table VI). Discussion I. F u n c t i o n o f T u b e - S h a r i n g

In mass culture dishes most mature animals were found in individual tubes. When two mature individuals were found in the same tube, they were always a heterogametic pair. Three or more animals were never found in the same tube, and males were more likely to be outside a tube than were females.

Table V. Sexes of Combatants of Contests that Occured When a Female that Had Just Been Tube-Sharing was Introduced to a Tube Containing a Tube-Sharing Pair

Female-female Male--female contests contests Female attempts entry at female end Female attempts entry at male end Totals

Totals

7 9

0 9

7 18

16

9

25

BOROWSKY: TUBE-SHARING IN MICRODEUTOPUS GRYLLOTALPA

795

Tube-sharing was transitory. Although there was much variation in the length of time a given pair shared a tube, in all the pairs observed for two weeks there was always a time when the two animals occupied different tubes. Most females tube-shared 12 h before they moulted. By 24 h after the female moulted, most males left the tubes. However, there was no relationship between the time of tube-sharing and the time of the males' moult. I suggest that the pattern of heterogametic tube-sharing observed here is the behavioural analogue of precopulation behaviour in the epibenthic species. Tube-building amphipods require the presence of a male at the time o f the female moult, as do the non-tube-builders. In the epibenthic species a heterogametic pair is fixed to each other to ensure the presence of the male at the female moult, but in M. gryllotalpa a heterogametic pair is fixed instead t o the same site at the time of the female moult. The alternation of tube-sharing and non-tube-sharing periods maximizes,resource utilization for this species. Casual observations of feeding behaviour showed that animals grasped food items that passed near the entrances of their tubes and drew the food into the tube, where it was eaten or glued to the tube to be eaten later. Occupants frequently turn around within the tube. Theoretically, single occupants have access to food that passes by both entrances, but tube-sharing animals, being restricted to only one entrance at a time, may have access to half the amount o f food that would b e available to them if they occupied t w o separate tubes.

larger animal generally wins a physical contest and (2) the drive to seek shelter is great in this species, and if the only shelter available is a tube with an occupant, the introduced animal will attempt to enter the tube anyway. When non-tube-sharing females were introduced to males' tubes, the results were different. First, tube-sharing, as opposed to contests, resuited significantly more often than when males were introduced to females' tubes. Second, the winners of contests were generally the occupant males, not necessarily the larger individuals. Among all animals, males contested males and females contested females, and the winner was generally larger. Further, in tests in which an introduced female attempted to enter a male's tube, half the time tube-sharing resulted and half the time a contest resulted. However, the accepta n c e of a male into a female's tube depended upon whether the female was currently tubesharing or not: a currently tube-sharing female always permitted a male to enter her tube, but heterogametic contests usually occurred when the female was not currently tube-sharing. These experiments showed (1) that since animals of the same sex will not share tubes, there are never more than two individuals in a tube, and (2) that the female determines the time of tube-sharing. Thus, the females' behaviour is cyclic. The results suggest that the female's behaviour is cued by physiological changes that vary with her moult and/or reproductive cycle, since these three characteristics co-varied.

II. The Mechanism of Tube-Sharing

The present studies suggest the mechanism of tube-sharing in the field. After copulation, the male leaves the tube. This is probably due to behavioural changes in the females and the male; the female 9becomes non-receptive to tube-sharing after the moult and the male leaves voluntarily. Since in the present study (sections IIA2

IH. The Pattern of Tube-Sharing in the Field: a Hypothesis

Among animals currently not sharing tubes, when a male was introduced to a male's, a female to a female's, or a male to a female's tube, a contest usually resulted. The final occupant, in all three situations, was generally larger and introduced. This is not surprising, since (1) a

Table VI. Number of Times Females Permit Males To Enter, and Number of Times Males Permit Females To Enter, When Currently Tube-Sharing andCurrently Not Tube-Sharing

Tube-sharing Number of Number of entries tests Female permits male entry Mate permits female entry

Not tube-sharing ~ entry*

Number of Number of entries tests

~ entry

8

8

100

7

29

24

12

21

57

14

30

47

*Only those tests in which an introduced animal first encountered an animal of the opposite sex were included here.

796

ANIMAL

BEHAVIOUR,

and IIB3) males won most heterogametic contests, presumably a male could remain inside the tube and eject the non-receptive female if so indined. The male then cruises from tube to tube attempting to gain entry. If an encountered tube contains a single receptive female, tube-sharing occurs. If the tube contains a tube-sharing pair, a male-male contest results, and the larger male is generally the final occupant, along with the female. If the tube contains a single non-receptive female, a contest occurs in which the larger individual or the male is the final occupant. If the tube contains a single male, a contest occurs and the winner is the larger and/or the cruiser. Failing to gain entry, the cruiser may construct his own tube. The above hypothesis would explain: (1) why males accept females into their tubes about half the time and engage in contests about half the time whether the male is tube-sharing or not (Table VI); and (2) why the male of a tubesharing pair is most often encountered by another animal attempting to enter the tube. First, if it is usually males that cruise from tube to tube, then an occupant male would expect an intruder to be another male. Thus, occupant males encountering an introduced female can respond to her either as an intruder (who should be a male and thus contested) or as a female (who should be permitted to tube-share). The results (section IIB1) showed this ambivalence. Second, if it is usually the males that cruise from tube to tube, and females in the tube-sharing part of their cycle will accept males into their tubes, then it is left to the occupant male to prevent the introduced male from gaining entry. Thus the occupant male moves to the end of the tube where an introduced animal is attempting to enter. The costs and benefits of cruising are probably about equal in the two sexes. Female energy is expended primarily on tube-building and frequent moults and egg production, while male energy is expended primarily on cruising and on interactions with other individuals. Males assume the risk of predation, since animals outside the tube are visible but those inside are virtually invisible (at least to a human observer). However, while a female can produce a brood only about once a week, a male can copulate at least once a day (personal observation) so t h a t while cruising increases the male's risk of predation, it also increases his fitness by increasing the number of broods he can fertilize in a given period of time.

28,

3

IV. The Possible Role of Sex Pheromones The presence of female sex pheromones has been suggested for several species of crustacea (reviewed in Dunham 1978). Among the amphipods, they have been demonstrated in Gammarus duebeni (Dahl et al. 1970a, b) and suggested for Gammarus pulex (Hammoud et al. 1975). Both of these species exhibit precopulation behaviour as the time of the females' moult nears. But both are epibenthic, and probably do not remain at one fixed site on the substratum as does Microdeutopus gryllotalpa. Therefore, the female sex pheromone may serve as a means of locating a female as well as a signal that the female is receptive to precopulation. The design of the present study provides no information about the existence of a female sex pheromone in Microdeutopus gryllotalpa. However, such a substance, if present, might serve to guide a cruising male directly to the tube of a receptive female, thus minimizing the number of intra-species encounters unlikely to result in tube-sharing. Studies designed to determine whether a sex-specific and/or a species-specific pheromone are present in M. gryllotalpa are currently underway. V. Conclusion The same pattern of tube-sharing has been demonstrated for another domicolous gammarid, Ampithoe valida (Borowsky 1978). It is conceivable that this pattern may occur in other species with similar ecologies. Having established that the female's tubesharing behaviour is cyclic and covaries with her moult and reproductive cycle, it is now possible to explore the physiological mechanism for the control of these three covariables. Aeknowledgments I thank K. O. Morgan for permission to collect animals at Gateway National Recreation Area, Jamaica Bay, New York; Ann Frame for help in identifying species; J. Cresce for assistance in the laboratory; and R. Borowsky, L. Mantel, and L. Powers for a critical reading of the manuscript. This work was supported by a Jessie Smith Noyes Foundation Post-doctoral Fellowship and, in part, by a Grant-in-Aid o f Research from Sigma Xi. REFERENCES Borowsky, B. 1978. The relationship between tubesharing and the time of the female's molt in Microdeutopus gryllotalpa and Ampithoe valida (Crustacea: Amphipoda). Am. Zool., 18, 621.

BOROWSKY: TUBE-SHARING IN MICRODEUTOPUS GRYLLOTALPA Bousfield, E. L. 1973. Shallow-Water Gammaridean Amphipoda of New England. Ithaca, N.Y.: Comstock Publishing Associates. Daht, E., Emanuelsson, H. & yon Mecklenburg, C. 1970a. Pheromone transport and reception in an amphipod. Science, N.Y., 170, 739-740. Dahl, E., Emanuelsson, H. & yon Mecklenburg, C. 1970b. Pheromone reception in the males of the amphipod Gammarus duebeni (Lilljeborg). Oikos, 21, 42-47. Dunham, P. J. 1978. Sex pheromones in Crustacea. Biol. Rev., 53, 555-583. Hammoud, W., Comte, J. & Ducruet, J. 1975. Recherche d'une substance sexuellement attractive chez les

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gammares du groupe pulex (Amphipodes, Gammaridea). Crustaceana, 28, 152-157. Kaestner, A. 1970. Invertebrate Zoology, Vol. 111. Crustacea. New York: Interscience. Mills, E. L. 1967. The biology of an ampeliscid amphipod crustacean sibling species pair. J. Fish. Res. Bd. Can., 24, 305-355. Myers, A. A. 1971. Breeding and growth in laboratoryreared Microdeutopus gryllotalpa Costa (Amphipoda: Gammaridea). J. nat. Hist., 5, 271-277. (Received 6 April 1979; revised 28 September 1979; MS. number: A2296)