Dryomyza anilis

Dryomyza anilis
Dryomyza anilis
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Diptera
Family:	Dryomyzidae
Subfamily:	Dryomyzinae
Genus:	Dryomyza
Species:	D. anilis
Binomial name
Dryomyza anilis Fallén, 1820
Synonyms
Dryope liturata Robineau-Desvoidy, 1830 Neuroctena anilis Róndani, 1868 Dryomyza pallida Day, 1881 Dryomyza melanacme Kurahashi, 1981

Dryomyza anilis is a common fly from the family Dryomyzidae. It has recently been placed back in the genus Dryomyza, of which it is the type species. Dryomyzidae were previously part of Sciomyzidae but are now considered a separate family with two subfamilies.

The fly is found through a variety of areas in the Northern hemisphere of the world and has brown and orange coloration with distinctive large red eyes. The life span of the fly is not exactly known, but laboratory-reared males usually live between 28–178 days. As the fly progresses through various stages from egg to adult, its cephalopharyngeal skeleton changes as it matures.

Male flies of the species engage in territorial behavior, guarding carcasses to attract females with which to mate. Females lay their eggs on carcasses, fungi, and excrement as well as other substrates. Males are territorial over females as well, and conflicts over females are frequent. Females typically mate with multiple males. Mating occurs through a series of rounds of copulation and oviposition, typically between 1 and 6 bouts. During mating, D. anilis males can be observed tapping their claspers on the female's external genitalia. This behavior significantly increases mating success for males, but may be detrimental for females.

Description

D. anilis adults are medium-sized, ranging in overall length from 7–144 mm, but are typically 12 mm long. Their coloration is light brown and orange with large red eyes. Generally, the species can be separated from other species of Dryomyzidae by their nearly-bare arista (apical bristle), covered lunule (a crescent-shaped mark, found around the wing margins), and developed prostigmatic and prescutellar bristles.

Dryomyzidae are characterized by closely-spaced first antennal segments, a protruding oral margin, a strap-shaped or oral prosternum that is not joined to the propleura, and a lack of costal spines. D. anilis have short posterior spiracular tubes, lack hooks on their posterior spiracular plates, and have well-developed tubercles on segment 12 only.

The fly's life span is between 28-178 days in the laboratory.

Morphology

Adult morphology indicates that Dromyzidae, Helcomyzidae, and Helosciomyzidae are more closely related to each other than they are to Sciomyzoidea. Therefore, though Dryomyzidae were previously part of Sciomyzidae, the family is now considered separate and has two subfamilies: Dryomyzinae and Helcomyzidae.

Moreover, as compared to other Dryomyza species found in the eastern United States (Dryope decipita and Dryomyza simplex), D. anilis is the most common species and has the strongest wing markings.

Distribution

This is a Holarctic fly, present in Canada and many northern states of the United States in the Nearctic. The fly is also widespread in the Palearctic from the United Kingdom to Japan.

Within the United Kingdom, the fly is common and widespread in England and Wales, but fewer occurrences have been noted in Scotland. D. anilis are typically most prevalent in the wild from the months of May–September.

Habitat

Dryomyza anilis in its natural habitat: low-laying, moist vegetation

Adult flies are found in moist, shady habitats among low-growing vegetation and excrement. D. anilis can develop from egg to pupa on dead animal matter but not on decaying plant matter. For example, experiments with larvae showed that they were unable to attain maturity when grown on rotting grass, decaying pumpkin flesh, decaying lettuce, or cow manure. They did attain maturity when grown on a hamburger, dead earthworms, dead crane flies, dead polygrid snails, a dead milkweed caterpillar, a dead slug, and rotting agaric mushrooms.

Adult habitats have been found in human excrement, fox and pheasant carrion, and malodorous stinkhorn fungi. Eggs have been found in human excrement, and larvae have been found in pheasant carrion.

Home Range and Territoriality

One of the defining characteristics of D. anilis is the territorial behavior found in males. Male territorial behavior supports the theory that these flies primarily view territory as a means to obtain females. However, males can obtain females without possessing territory. Males will defend small carcasses or feces where females arrive to feed and lay their eggs, and fights over these resources are common between males of the same species.

Territory-based conflict take-overs

Some of these territory-based conflicts result in take-overs, in which a male is displaced from either the territory or the female and replaced with another male fly.

In one study, 53% of contests over females and 39% of contests over territory resulted in such a take-over. The owners were, on average, smaller than the territory owners or copulating males, respectively. Differences in resource holding potential played into the outcome of these take-overs. These factors include differences in size, weight, position, and payoff asymmetry (having more or less to lose than the other involved party). The relative size of the female and her resource value, i.e. her egg content, plays a role in the evaluation as well. Some of the variability in outcome can also be attributed to uncorrelated asymmetry, such as in situations where a newcomer decides to respect the previous male's ownership of the resource, and retreats. For instance, it was observed that the second attack by an intruder lasts only half as long as the initial encounter, implying that useful information about relative fighting ability is obtained and processed through encounters. The male is able to identify his superiority or inferiority in relation to a second male, and gauge the amount of effort that should be invested in response.

Size of male

Of the aforementioned factors, size of the male shows the strongest linkage to winning in a male-male conflict over resources. Copulating males are larger than average males, but still smaller than territorial males. Therefore, some non-territorial males must still have access to females. On carcasses less than 100 g in weight, a single male is able to establish territory. Territorial males are generally much larger than other males on average, and territorial males are able to move and attack other males more frequently than non-territorial males. Take-overs often continued in a process whereby resource owners continue to change hands until one is strong enough to successfully fend off the territory from future threats.

Contests over females

In Otronen's 1984 study, contests over females lasted longer than those over territories. This finding suggests that males view females as a more valuable resource—one worth expending more time and energy over—than territories. In particular, large carcasses attract more males than smaller ones. However, once the density surpasses a certain stage, fewer males will attempt to take control of a certain territory; taking advantage of territorial behavior decreases as the intensity of competing males increases.

Life History

Egg

The egg is a creamy white shade with an elongated shape and is somewhat tapered anteriorly. Dorsolaterally, paired, elongated, ribbon-like flanges are present. The ending of each flange is anteriorly rounded and more acute on the posterior end. The dorsal surface of the egg is covered with fine, radiating ridges. There are more small curved flanges present on the anterior and posterior sides of the egg. The surface of the egg, apart from the lateral flanges, is covered in a fine, honeycomb-like reticulation. The structure of the egg is well-adapted to survival, given the kinds of substrates upon which eggs typically are laid. The series of flanges that the egg has allow it to float on the surface of a liquid or semi-liquid substrate, as is often the case.

Larvae

First instar

The length of the instar ranges from 1.67–2.96 mm, with a maximum width of around 0.41–0.59 mm. Anterior spiracles are not yet present, while posterior spiracules are pale yellow, and each has a B-shaped spiracular opening. Four sets of peripheral palmately-branched hair-like processes (about half as long as the diameter of the plate) are present.

An important component of fly anatomy is the cephalopharyngeal skeleton. The skeleton usually has one or two mouth hooks to allow the fly to move and feed. As the fly matures, cephalopharyngeal skeleton also changes to maximize the fly's ability to take in nutrients. The cibarial dilator muscles connect to the skeleton to lift the roof of the pharynx and thereby widen the lumen. At the first instar stage, the cephalopharyngeal skeleton is brown-black in color and 0.28–0.33 mm long.  The segments vary in pigmentation but contain 3–4 rows of dark pigmentation and are followed by a series of smaller, colorless spinules that extend laterally from each side of the midline ventrally. Paired sclerites (associated with oral grooves) present below the rows of spinules. Lateral bars fuse to form a mouth-hook-like structure, and each bar fuses posteriorly to the edge of its respective sclerite. Another series of weakly-fused sclerites presents below the anterior ends of the lateral bars. Some pharyngeal sclerites without windows are present, a pigmented bridge exists anterodorsally, and pharyngeal ridges are present between the ventral cornua.

Second instar

The second instar stage is similar to the third instar larva. The length at this point ranges from 2.74–4.71 mm, with a maximum width of around 0.61–0.91 mm. Anterior spiracles are now present and are also colored a pale yellow. Posterior spiracular plates are pale yellow-brown, each with two elongate spiracular slits, a white spiracular scar, and four sets of peripheral, palmately branched, hair-like processes that are about a third as long as the diameter of the plate. There is a ventral spiracular plate upcurved at both ends.

The cephalopharyngeal skeleton is 0.57–0.61 mm in length. Mandibular sclerites exist as long, narrow, mouth-hooks that appear triangular from the lateral view. The sclerites bear 3–4 ventral teeth in the anteroventral view, connected the mandibular sclerites by bars. Dentary sclerites are pointed ventrally, and are lightly pigmented posterodorsally. Small sclerites are present in between the mandibular ones, and a hypostomal sclerite with a posterior end is present. Pharyngeal sclerites have progressed to display narrow windows posteroventrally and posterodorsally, on the dorsal and ventral cornua, respectively. The bridge is present anterodorsally, and pharyngeal ridges are between the ventral cornua.

Third instar

At the third instar stage, length is between 4.10–9.42 mm and greatest width is between 0.76–2.13 mm. The integument is translucent, the body becomes shaped in a conicocylindrical fashion, and the anterior end becomes strongly tapered. The posterior end becomes truncated and has a strong slope. Tubercules are no longer present from segments 1–11. The following characteristics are present in various stretches of segmentation:

• Segment 1: bilobed apically, and each lobe has a short, pale yellow-brown sensory papilla and a pair of circular sensory plates. Oral grooves are present. The posterior portion is covered in fine spinules
• Segment 2: paired, yellow-brown, reniform, and with transverse anterior spiracles posterolaterally. Spiracles project almost perpendicularly to the body, each with 19–24 papillae
• Segments 2–3: have fine, colorless spinules that are especially dense in the dorsal and anterior regions
• Segments 4–11: covered in larger, yellow-brown spinules dorsally and laterally, with more density at the anterior end of each segment ventrally
• Segments 5–11: have poorly developed fusiform welts posterolaterally
• Segment 12: covered in spinules, bearing anal plate, paired with anal lobe, minute ventromedial lobe, and spiracular disk posteriorly

The cephalopharyngeal skeleton is dark brown-black and 0.93–1.05 mm long. Mandibular sclerites are well-developed, paired, and separate, without the accessory teeth present. Dentary sclerites are paired and separate near the margin of the mandibular sclerites. Epistomal sclente are not fused with parastomal bars and are located between anterior rami of the hypostomal sclerite, loosely articulated with strap-like sclerites. The parastomal bars have narrowed and are darkly pigmented, with their posterior ends fused to pharyngeal sclerites. The hypostomal sclerite is not fused and has anterior rami that are wider than its posterior rami. The hypostomal bridge is notched posteriorly. Small, paired sclerites are between the anterior rami of the hypostomal sclerite and the dentary sclerites. Pharyngeal sclerites with an anterodorsal bridge joining anterior ends of the dorsal cornua are present, and there are anteroventral projections below the posterior rami of the hypostomal sclerite.

Food Resources

D. anilis can survive on variety of food sources ranging from insects and vertebrates to rotting fungi. The well-developed pharyngeal ridges in the skeletal structures of all three larval stages suggest that larvae derive nutrition from materials such as micro-organisms that are able to colonize the rotting organic food source. The ridges can separate bacteria and other micro-organisms from liquid that enters the pharynx. Through this mechanism, the fly is able to control which materials are taken up to ensure that only nutritious food enters. Larvae that feed on living tissue do not have these pharyngeal ridges.

Anatomy

Reproductive anatomy

The female sperm storage organs consist of a single bursa copulatrix and three spermathecae that are attached to two spermathecal tubes, forming a “singlet” and “doublet” spermathecal unit. The spermathecal tubes are relatively narrow, and communicate with the vagina. The narrow diameter of the female ducts means that the male aedeagus cannot enter. During intromission, the male aedeagus is inserted into the bursa copulatrix. During tapping, the male claspers grab the region around the female's external genitalia, bearing short, stout cuticular bristles that have ball-like basal joints. These bristles have the characteristic mechanoreceptive sensillae structure.

During male tapping, more sperm moves into the singlet spermatheca. The total number of sperm correlates positively with the sperm number in all storage organs, i.e. if more male sperm enters the female overall, then the female's various reproductive organs will also contain more sperm. Male size also correlates positively with the number of sperm remaining in the bursa. The number of sperm increases with increased number of matings only in the doublet spermatheca. This indicates that in the singlet spermatheca, the sperm were either replaced by another male, or that the sperm originally never reached the organ. During egg laying, females were found to use sperm primarily from the singlet spermatheca. These results illustrate a differentiation in function between sperm storage, and sperm usage, for different female reproductive organs.

Mating

In mating, the male D. anilis fly mounts the female, and facing the same direction as her, persuades her to spread her wings. He facilitates this process with the assistance of the tip of his abdomen and hind tarsi. Meanwhile, his fore tarsi are placed either on the substrate or on the female's head, his mid tarsi are on the substrate or the base of the female's wings, and his hind tarsi grasps the female's abdomen near the midlateral line of segments 3 and 4. Throughout the entire duration of mating, the male's wings are in the resting position.

Dryomyza anilis adult male

Males mate differently with females depending on whether or not they have mature eggs. Males are able to assess the egg content of a female by pressing his hind legs against the female's abdomen and rejecting her if she does not have mature eggs. Overall, male flies tend to spend less time with females who do not have mature eggs. This may have developed as an evolutionary mechanism to maximize the male's reproductive success. Females with more eggs were also more successful and had more copulation bouts than the females with fewer eggs.In addition, males required more tapping sequences or copulation bouts when mating with a female who had many mature eggs in order to obtain the highest possible average gain rate.Males needed to make a consideration in balancing the costs and benefits of providing their sperm to each female. If the male gives up too much sperm, sperm depletion can result. The male's future matings will then include fewer copulation bouts.

Experiments have shown that the male places his sperm near the exit of the female's bursa copulatrix. Most of the last male's sperm is typically expelled by the female before oviposition, as only 10–30% remains. Therefore, it will benefit the male to be the last one to mate with a given female. There seems to be a cumulative percentage increase in fertilization for the final male, such that the eggs laid in the last oviposition bout are the most successful. To begin the first copulation bout, the male and the female walk away from the carcass. Each mating consists of about 1–6 copulation and ovulation bouts which alternate back and forth. Only a few eggs are laid by the female before the pair leaves the carcass to return to another copulation bout.

Copulation

Copulation begins with insertion of the male's aedeagus into the female's genital tract. The two will remain motionless for a moment, and then the male initiates a series of tapping movements. The male taps his claspers on the female's external genitalia. This occurs about 20 times, but one mating can contain anywhere from 8–31 tapping sequences. Most of the tapping occurs during the first copulation bout. Between tapping sequences the pair is motionless. Ultimately, the sequence terminates with a single, longer period of contact. Tapping significantly increases fertilization success, especially for the final male. If females are first mated with a normal male and then with a sterile male, the last male can increase his percentage fertilization within a copulation bout from 18% to 70% by increasing his taps from 0 to 25 sequences.

While tapping, the male's claspers are touching a special portion of the female's abdomen containing mechanoreceptive sensillae. The exact mechanism of tapping increasing fertilization success is unknown, but it has been theorized that tapping movements could induce sperm precedence by affecting the female's genital muscles. The exact amount of time spent in copulation does not affect fertilization success, but spacing out the time in between the end of a copulation bout and the start of an oviposition bout positively correlates with fertilization success. With more rounds of tapping, more eggs were laid as well. Therefore, the male should seek to go through multiple cycles of copulating and ovipositing with the female in order to maximize success. For individual males, the number of tappings per sequence was positively correlated with higher fertilization success. However, in matings with an unlimited number of tapping sequences, fertilization success depends on female resistance.

Sperm competition

The mechanisms of sperm competition practiced by male D. anilis flies are similar to those present in many other species. For instance, sperm removal occurs when the male physically removes another male's sperm from the female's sperm storage. In sperm displacement, the rival male's sperm is moved aside. Sperm mixing is the mechanism through which males are able to dilute other male's sperm by flooding the female reproductive tract with their own. This increases the probability that their sperm will be the one to fertilize the female's eggs. However, female choice is also present. The fast and divergent evolution of male genitalia could have been influenced by female mating preferences. Only males that are able to stimulate the copulating female best will be able to attain insemination.

Males do not need to maximize their gain rate in each individual mating, but rather should seek to maximize their average gain over several matings. Meanwhile, males should continue one particular mating only as long as the cumulative gain attained in terms of percentage fertilization is above the expected average gain rate attained by withdrawal from the mating, in order to start a new one. Ideally each male should tailor his mating strategy depending on the female.

In take-over situations, there is intensified sperm competition for the second male who mates with the female. This occurs because the female cannot discharge the sperm inseminated by the first male as she normally would do with a new mating. The reduced fertilization success for the second male is between 8–10%, while the first male's fertilization is 7–14% higher in take-overs. Even though the intruder is larger than the paired male, his superior fertilization success often does not compensate for the effect of the sperm that is already present within the female. Therefore, males often compensate by increasing their rate of tapping in order to increase fertilization success. Higher fertilization success for the first male after a takeover is especially significant for the reproductive success of small males. These males often lose their females to larger males.

Female resistance

Females frequently resist tapping sequences during matings. In nature, females avoid consecutive matings to keep oviposition as continuous as possible. Lone males will attack mating pairs and take the female before oviposition can occur or during the oviposition bout. Large females may be better at resisting in these scenarios, but large males are also better at countering female attempts to resist.

There are a variety of conflict behaviors that have been observed during mating:

• Walk and turn: likely that only the female can walk, although the male may be able to direct the walk to some extent with his middle legs (usually, the male has only his middle legs free because his hind legs are grasping the female's abdomen and his front legs are holding her by the head)
• Shake: quick side-to-side shaking movement during which the male usually strikes the female's abdomen with the tip of his abdomen
• Roll: resembles a struggle, where pair loses balance and rolls on the ground
• Abdomen down: female resistance
• Fluttering wings: performed by the male before the pair is about to leave the carcass
• Extra intromission: performed by the male under female resistance; usually only one intromission at the beginning of each copulation bout
• Kick: female tries to push male's abdomen away with her hind legs. This takes place before an intromission.

Factors influencing fertilization success

Large females spend less time mating and have fewer copulation bouts than smaller females. Similarly, large males typically have more tapping sequences per mating than smaller males. Male asymmetry is also related to fertilization success, as measured in terms of wing length, tibia length, and the length of  the small and large claspers. Fertilization success is also negatively correlated with the fluctuating asymmetry of wing length, suggesting either that females have a preference for more symmetrical males or that there is a relationship between male asymmetry and intrasexual selection. Fertilization success decreased with an increased length of claspers, and males with asymmetrical small claspers enjoyed higher fertilization rates than those with symmetrical claspers.

Percentage fertilization is also positively correlated with the amount of time spent in the copulation bout before oviposition. This indicates that males might increase their percentage fertilization simply by delaying oviposition. This is important if the sperm are moving between different female sperm storages due to the interference of other males. There is also a negative correlation between the length of intromission and percentage fertilization. Moreover, the fewer eggs laid by a female after a copulation bout, the higher percentage fertilization was among these eggs.

Conflict between males and females

Repeated copulation is a strategy males use to maximize fertilization, but females are likely to favor matings with quick oviposition. Females can store sperm for at least two egg batches without fertilization rate decreasing, and mating before each oviposition is not necessary for her. However, due to frequent take-overs and other conflicts between male flies, females end up mating with several males before oviposition is completed. Repeated copulation may have been a mechanism that developed in connection with males trying to secure their paternity, as females are able to discharge sperm during any point in mating.

There are certain benefits for females engaging in polyandry. The female can exchange the benefits offered from resource-holding males for her cooperation in copulation. She gains nutrition from the sperm and access to feeding and oviposition sites. These must be balanced with the costs of mating, specifically the time and energy that mating involves, risk of predation, disease, and injury in intra-sexual conflicts. In mating systems where males are able to control the resources, females are more likely to have a restricted choice of males. However, overall, there is no significant benefit for females in multiple matings. Large females are at an advantage as they often participate in fewer matings.

Parental Care

After the tapping sequences of mating, the male and female return to the carcass in order to prepare for oviposition. Females benefit from males guarding her during oviposition; this is another reason that large males may be favored. Before oviposition, the female has been observed to expel a droplet of sperm from her genital orifice.

Egg laying

Eggs are laid one at a time and are rarely deposited onto a dry surface. The lower surface of the egg is shiny and sticky. Eggs are sometimes deposited side-by-side. The incubation period for eggs is relatively short, typically around 24 hours. At eclosion, the chorion at the anterior end of the egg splits, and the larva escapes. The young larvae then search for a soft spot or crevice into which they can burrow, leaving only the posterior spiracles exposed.

Enemies

The short incubation period of the fly (around 24 hours) may provide a competitive advantage in exploiting limited resources. Moreover, the fly is able to prevent parasitism or predation at a key stage. No predators or parasites of D. anilis have yet been studied, but it has been reported experimentally that several larvae of Mydaea urbana destroyed a large population of D. anilis on human excrement.

Protective Coloration and Mimicry

The chorion takes on the color of the substrate that it is laid on, affording the egg camouflage and protection from predators. The fly itself is not known to demonstrate any other protective coloration or mimicry behaviors.

Conservation

There is evidence that Pacific salmon function as a food source and egg-laying substrate for D. anilis. Therefore, the interactions between salmon and the fly species can be used as a mechanism to measure ecosystem health.

Pacific salmon allow for subsidization of terrestrial communities around them with their marine-derived nutrients and energy. They provide a predictable source of protein in particular and supply hundreds of species throughout the coastal areas of the North Pacific.  In aquatic systems, the retention of salmon carcasses can feed nitrogen, phosphorus, and other nutrients into the environment. These processes initiate bottom-up food web effects. Live and dead salmon support a wide array of organisms, with D. anilis being one of these key species.

D. anilis’s ecological role in the system was classified as a saprophage. Together with Calliphora terraenovae, these two species dominated adult collections found in baited traps. These species have also been collected from salmon carcasses in Alaska, highlighting that they have significant interactions with spawning salmon and are key to understanding further consumer interactions. There is concern that continued decline in these salmon populations can threaten salmon-dependent communities, and impact the survival of species such as D. anilis, as well as the well-being of the larger ecosystems and communities surrounding them.