How Many Matings are Necessary for Varroa Mites?
Gerard Donze, Institute of Zoolgy , University of Neuchatel, Switzerland, Peter Fluri, Anton Imdorf, FAM, Liebefeld, Switzerland.
Translated from the Deutsches Bienen Journal 2/98 pp 11 –13,
by A.E.McArthur MIL.
During the reproductive period in the sealed brood cell of the honey bee the Varroa mite exhibits a highly organised behaviour pattern. The mites appear to strive for good reproductive success, without inflicting excessive damage on the host. In the January 1998 issue of the “Deutsches Bienen Journal” we described in detail the events in the brood cells. Here we want to continue with these observations to explain why the young female mites mate so often with the single male mite produced, before they leave the cell with the emerging bee.
Overview of the Reproductive Cycle of the Varroa Mite
The beekeeper only sees the female mite, which uses the adult bee for transport, in the work of the hive (phoretic stage). The mites transfer from the adult bees to the brood cells. about to be sealed, for the reproductive stage. The young mites are born and nurtured here. The mated mites leave the cells with the emerging bee. The mite then remains on the adult bee before she transfers herself to a suitable brood cell for the reproductive stage. Many female mites repeat the reproductive cycle a number of times. The male mites on the other hand only live in the sealed cells and die when the host emerges. The development and behaviour of the mite is optimally suited to the life cycle of the host honey bee. Without this close relationship the parasite would not be so successful.
In each cycle the mite lays 5 – 6 eggs at intervals of 30 hours. The first egg produces a male mite, the subsequent eggs all develop into females. The male as first born is sexually mature and mates with the first female as soon as she is mature. Thereafter every 30 hours another female mite matures, she is immediately mated many times by the male mite. The concentrated mating behaviour in favour of each female progeny is advantageous for the reproductive success of the species. It is critically important for the females that they are mated by a brother or the male progeny of another Varroa mother in the same cell before they leave the brood cells, because the male mites cannot exist outside the brood cells. Young female mites not mated before the emergence of the host remain sterile. The rate of increase is therefore linked to the length of time the cell is sealed. The mite success is due among other things to its highly developed house-keeping behaviour in the brood cell. The mother mite deposits a cluster of faeces at the back of the cell on the cell face above the abdomen of the honey bee larva. Later all of the progeny will deposit their faeces on this same spot. This point then becomes the focal meeting place for the whole mite family. This behaviour ensures that the young females mites and the male mite meet directly after each female mite reaches maturity. Of the 287 matings observed 90% occurred either on the faeces deposit or at its edge.
The Mating Act – a Programmed Succession of Actions
The only preparation consists of the male mite cleaning the chelicera (mouth parts) and pedipalps (sensory extremities close to the mouth). From it may be seen that the chelicera has a tube like form. The male uses this later to take up sperm from the sexual orifice in the middle of his abdomen and transfer it to the abdomen of the female. At the start of the mating act the male climbs onto the back of the female and moves in the direction of her mouth. At this position it turns around and feels along the side edge toward the rear of the dorsal plate. This edge carries a row of prominent hairs. When the male reaches the anal area which is devoid of hairs he crawls under the stomach of the female. The female assists here by raising her body. The male then touches the stomach of the female with the pedipalps and the front legs, moving many times from one side to the other. He then remains in the middle, addresses his mouth parts to his own genital opening, until a sperm globule , in the form of a shiny ball appears (sprematophore) appears. He takes this in the chelicera and moves to the side, to place the sperm in the sexual openings (solenostom) of the female, these are located on both sides between the bases of the 3rd and 4th pairs of legs. From this position later on they come into contact with the eggs which they then fertilise. The first egg is of course not fertilised (parthenogenic development of the male mite).
Most mating acts (71%) last less than 3 minutes. There were uncompleted attempts, which were broken off prematurely. Sperm was only transferred in the 26% of matings which lasted more than 6 minutes. The complicated mating procedure ensures that the female being mated is the correct one, that is a young hetitlehy female and that the male mite is also hetitlehy. From observations it has been established that the male is able to differentiate young mites from the older females in that matings with the mother mite or older daughters are broken off. This graph furthermore shows that the first mating act with a new young female occurs immediately after its arrival at the faecal meeting point. The matings are continued unabated thereafter.
Frequent Matings are Necessary for a High Fecundity
Because there is only one male mite per mother mite it might be expected, that his limited sperm quota would be equally distributed between all future sisters. Our observations have however indicated otherwise: The male mates with the first sexually mature female immediately and as often as possible until the second female is mature. Mating with this second female only, continues until the arrival of the third female and so on. The graph shows a typical model of the frequency of mating: The first three sisters mated eight, four and two times respectively. The third sister is unable to be mated more than twice due to the host bee beginning to emerge. We questioned ourselves as to how the male mite obtained the nourishment necessary for the formation of the abundant sperm quota. We observed that he frequently sucked larval blood at the communal feeding hole made by the mother mite in the larval skin. The mouth parts (chelicera) which are transformed to transfer sperm, in no way inhibit the male mite’s ability to feed itself similar to the females at the feed hole.
How much Sperm does a Female Accept?
To answer this question we carried out the following experiment: Using transparent worker cells we allowed two young Varroa females to mature sexually, with no male mite present. Later on two male mites from natural brood cells were introduced and events observed using a binocular microscope connected to a video camera in a brood chamber (34 C, 60% Relative humidity). Each mating act lasting longer than 6 minutes was considered to be successfully completed. Three test groups were formed: (A) females which were only mated once, (B) females which were mated twice and (C) females which were arbitrarily mated over a period of 48 hours. Mother mites from sealed cells were used as a control group (D). Three days after the matings had occurred the sperm was able to be found in the spermatheca of the female mite. The initially have a pear shaped form and later become thread like. In order to count the sperm the females were dissected in a physiological stitle solution. The spermatheca was removed and the sperm contained therein was counted under the microscope. The results showed none of the five females which were mated only once had any sperm in the spermatheca. Opposed to this the 14 females which mated twice had between 0, (5 females) and 26 sperm. With the exception of one female the eleven females which were arbitrarily mated during the 48 hour period had more than 24 sperm and three females had over 40 sperm. Earlier researchers have found similar numbers. Their results however showed maximum values of less than 40 sperm per spermatheca. These results correspond to the apparent sperm requirement of a mother mite during her life. Research by other authors indicate that such a female, performing a maximum of 5 – 6 reproductive cycles will fertilise a total of approximately 30 eggs. The sperm necessary for this must be taken up by the spermatheca of the young newly sexually mature female, during the repeated mating acts.
Our observations have shown that the young females in the sealed broods cells have a time limitation on them in their need to obtain the necessary number of matings. The excrement pile performs the function of providing a constant meeting point for all of the mites thus saving valuable time for the necessary mating acts to give the required sperm count. Repeated mating acts are necessary to fill the spermatheca with the approximately 30 sperm required by the mature sister. The male mite exhibits a behaviour pattern which complements this requirement: He always prefers the youngest most recently mature female to all the older females. So long as no new young female arrives at the meeting point he mates continuously with the current youngest female. Mating acts with older females are broken off prematurely. Due to this behaviour the greatest possible fecundity of each sister mite, which becomes mature even up to a few hours prior to the emergence of the host honey bee is achieved.