Prey features affecting ingestion rates by Acanthocyclops robustus (Copepoda: Cyclopoida) on zooplankton

Summary (1) Ingestion rates by adult female and juvenile Acanthocyclops robustus on a number of prey types were measured at a prey concentration of 100/l in experimental volumes of 300–400 ml. (2) For the adult predator, Synchaeta pectinata was most vulnerable (22.3, standard error 1.4, prey ingested per predator per day) as compared to Brachiomus calyciflorus, Brachionus diversicornis, Keratella cochlearis (two morphs), Asplanchna priodonta, Polyarthra major, Synchaeta kitina, Pompholyx sulcata, Daphnia spec., and Bosmina longirostris. For these latter prey, the lowest ingestion rate was on one morph of K. cochlearis and the highest on A. priodonta, being, respectively, 1.0, SE 0.5, and 11.3, SE 1.0, prey per predator per day. (3) With regard to the juvenile predator (mostly copepodite stages I, II and III), ingestion rates on K. cochlearis and P. sulcata were low (respectively 1.2, SE 0.7, and 0.3, SE 0.1, prey per predator per day) but quite high on S. kitina (5.7, SE 0.6). (4) In addition, the effect of increasing prey concentration on the ingestion rate (functional response) by the adult female predator was examined for B. calyciflorus, K. cochlearis, S. pectinata, S. kitina and Daphnia spec.. Increases in ingestion rate with prey density were minimal for B. calyciflorus and K. cochlearis, greater for Daphnia spec., still greater for S. pectinata and of greatest magnitude for S. kitina. (5) The reasons for these results are discussed with particular reference to prey features.     

Some aspects of vulnerability to cyclopoid predation of zooplankton prey individuals

The predation cycle (encounter, attack, capture and ingestion or survival) by adult female Acanthocyclops robustus was observed for four crustacean prey types. The chief defense of A. robustus nauplii was escape response ability, reducing the probability of capture after attack, and, most likely, attack after encounter. The most important feature reducing the vulnerability of Ceriodaphnia and Daphnia species was large body size, decreasing the probability of capture after attack. Escape response ability and carapace strength/integrity further reduced vulnerability. Carapace strength/integrity was an effective defense for Bosmina longirostris, reducing the probability of ingestion after capture.The predation cycle by juvenile A. robustus was examined for three prey types. All three prey types seemed to be readily attacked. Due to their possession of loricae, Keratella cochlearis and Pompholyx sulcata were seldom eaten, while the illoricate Synchaeta kitina was highly vulnerable.Egg vulnerability after attack by the adult female predator was analysed. The eggs of Brachionus calyciflorus, Pompholyx sulcata and Filinia longiseta were rarely eaten, although the adults of the latter were usually ingested (thus causing the eggs to float free). Out of three attacks recorded on Keratella Quadrata, the eggs were eaten (or destroyed) twice.Handling times by the adult female predator were measured for a number of prey types. The shortest mean handling time was for Synchaeta kitina (less than one second), while the longest was on Ceriodaphnia species (716 seconds). Results were quite variable. Handling time was significantly positively related to prey body volume, while exoskeletal strength/integrity also increased this time. No effect of temperature on handling time was found for Synchaeta pectinata or Polyarthra major between 15 and 26.5 °C.     

Generation time of Acanthocyclops robustus in relation to food availability and temperature in a shallow eutrophic lake

The generation time of the predatory cyclopoid copepod Acanthocyclops robustus was estimated on 11 occasions during the years 1980 to 1982 in Alderfen Broad. In a multiple regression model, generation time was found to be uncorrelated with temperature, positively correlated (p < 0.05) with the densities of Bosmina longirostris and rotifers, and negatively correlated (p < 0.001) with the density of nauplii of the calanoid copepod Eudiaptomus gracilis. It is suggested that generation time was determined largely by the availability of calanoid nauplii as prey, even though these constituted only 2% of zooplankton standing biomass.     

Effect of selective planktivory by fry of Rhamdia sapo (Pimelodidae: Pisces) on zooplankton community structure

SUMMARY.

• 1 The direct and indirect effects of predation by larval fish (Rhamdia sapo) on zooplankton in rearing tanks are analysed. Rhamdia sapo larvae showed an unusual species-selectivity for Acanthocyclops robustus, the main invertebrate predator present.
• 2 Acanthocyclops robustus populations were markedly reduced, presumably as a direct consequence of species-selective removal. Other zooplanktonic prey were not significantly affected by R. sapo predation.
• 3 Rotifers increased in tanks with fish, but this was not related to herbivorous crustacean variables (biomass, mean weight, abundance and species composition). On the contrary, rotifer biomass was negatively correlated with some A. robustus variables (biomass and mean weight of adults + copepodites and nauplii biomass). Thus, the rotifer increase appears to be an indirect effect of predation on A. robustus by R. sapo larvae.

     

Habitat selection and diel distribution of the crustacean zooplankton from a shallow Mediterranean lake during the turbid and clear water phases

1. The fish fauna of many shallow Mediterranean Lakes is dominated by small‐bodied exotic omnivores, with potential implications for fish–zooplankton interactions still largely unknown. Here we studied diel variation in the vertical and horizontal distribution of the crustacean plankton in Lake Vela, a shallow polymictic and eutrophic lake. Diel sampling was carried out on three consecutive days along a horizontal transect, including an open‐water station and a macrophyte (Nymphaea alba) bed. Since transparency is a key determinant of the predation risk posed by fish, the zooplankton sampling campaigns were conducted in both the turbid (autumn) and clear water (spring) phases. 2. In the turbid phase, most taxa were homogeneously distributed along the vertical and horizontal axes in the three consecutive days. The only exception was for copepod nauplii, which showed vertical heterogeneity, possibly as a response to invertebrate predators. 3. In the clear water phase, most zooplankton taxa displayed habitat selection. Vertically, the general response consisted of a daily vertical migration (DVM), despite the limited depth (1.6 m). Horizontally, zooplankters showed an overall preference for the pelagic zone, independent of the time of the day. Such evidence is contrary to the postulated role of macrophytes as an anti‐predator refuge for the zooplankton. 4. These vertical (DVM) and horizontal (macrophyte‐avoidance) patterns were particularly conspicuous for large Daphnia, suggesting that predation risk from size‐selective predators (fish) was the main factor behind the spatial heterogeneity of zooplankton in the spring. Thus, the difference in the zooplankton spatial distribution pattern and habitat selection among seasons (turbid and clear water phases) seems to be mediated the predation risk from fish, which is directly related to water transparency. 5. The zooplankton in Lake Vela have anti‐predator behaviour that minimises predation from fish. We hypothesise that, due to the distinct fish community of shallow Mediterranean lakes, aquatic macrophytes may not provide adequate refuge to zooplankters, as seen in northern temperate lakes.     

Retarded growth of cladoceran zooplankton in the presence of a copepod predator

Various instars of four different cladoceran species representing a wide spectrum of body size were grown at high food availability in the presence and in the absence of natural densities of an invertebrate predator, a cyclopoid copepod Acanthocyclops robustus (G.O. Sars). Daily weight increments calculated from individual weights at the end and at the beginning of each 1, 2 or 4 day experiment, showed that individual growth was more or less drastically retarded in the presence of the predator as well as when exposed to water in which the predator had been feeding. The data also showed that the effect of this invertebrate predator was more pronounced in small prey instars and small prey species that were more vulnerable to predation than large prey.     

Near-bottom depletion of zooplankton over a coral reef II: relationships with zooplankton swimming ability

Intense predation by corals and associated fauna can generate vertical gradients of their zooplankton prey. The goal of this study was to characterize the small-scale distribution of zooplankton above the coral reef of Eilat, Israel. Four vertical arrays, each consisting five underwater pumps attached 0.5–3 m apart on a taut mooring, were deployed for 10 days at two sites over the reef slope. A distinct layer of depleted zooplankton was repeatedly found in the 1.5 m high benthic boundary layer. The gradient was sharpest for strong swimmers (copepods and polychaeta), intermediate for weak swimmers (nauplii, mollusks and appendicularia), and lacking for passive taxa (eggs and foraminifera). Spatio-temporal changes in the abundance of copepods and polychaetes were highly correlated, more so in the water aloft (Pearson r>0.9) than near the bottom (r>0.8). The spatio-temporal correlations between weak swimmers and between passive taxa were much weaker (r<0.8 and r<0.4, respectively). Flow and shear stress did not affect the distribution patterns. The correspondence between the zooplankton distribution and their swimming ability indicates that bottom avoidance contribute to the formation of depleted layer over the reef.     

Phytoplankton and zooplankton (Cladocera,Copepoda) relationship in the eutrophicated River Danube (Danubialia Hungarica,CXI)

The seasonal variation in primary production, individual numbers, and biomass of phyto- and zooplankton was studied in the River Danube in 1981. The secondary production of two dominant zooplankton species (Bosmina longirostris and Acanthocyclops robustus) was also estimated. In the growing season (April–Sept.) individual numbers dry weights and chlorophyll a contents of phytoplankton ranged between 30–90 × 10⁶ individuals, l^–1, 3–12 mg l^–1, and 50–170 µg l^–1, respectively. Species of Thalassiosiraceae (Bacillariophyta) dominated in the phytoplankton with a subdominance of Chlorococcales in summer. Individual numbers and dry weights of crustacean zooplankton ranged between 1400–6500 individuals m^–3, and 1.2–12 mg m^–3, respectively. The daily mean gross primary production was 970 mg C m^–3 d^–1, and the net production was 660 mg C m^–3 d^–1. Acanthocyclops robustus populations produced 0.2 mg C m^–3 d^–1 as an average, and Bosmina longirostris populations 0.07 mg C m^–3 d^–1. The ecological efficiency between phytoplankton and crustacean zooplankton was 0.03%.     

Vertical, lateral and longitudinal movement of zooplankton in a large river

1. The spatial distribution and movement patterns of zooplankton in large rivers are little known compared with those in lake environments. We conducted a series of studies in the Ohio River (U.S.A.) during the low flow period to assess diel vertical (DVM), longitudinal and lateral movement of crustacean zooplankton. 2. The dominant large zooplankter, the copepod Eurytemora affinis, showed a consistent vertical migration pattern of daytime ascent and night‐time descent during all sampling periods – the reverse of the most common migratory pattern of zooplankton in lakes. The cladoceran Bosmina migrated in a similar way in two of the three sampling periods. Surveys taken longitudinally in the river showed similar trends for both taxa. 3. During the lateral surveys, E. affinis was significantly more abundant in the shallow littoral zone during the night than in the daytime. The combination of vertical and lateral movement patterns along with the diel distribution of zooplanktivorous fish suggest that these movements are a predator‐avoidance mechanism. 4. Sampling programmes in large rivers should consider that larger zooplankton such as E. affinis may not be randomly distributed in the river channel and behaviours such as diel vertical migration may be just as evident in river habitats as in lakes.     

Day‐Night Vertical Distribution and Feeding Patterns of Fourth Instar ofChaoborus Larvae in a Neotropical Reservoir (Socuy Reservoir,Venezuela)

The day‐night vertical distribution, diel feeding activity and diet of fourth instar of Chaoborus larvae were analyzed in lacustrine zone of a neotropical reservoir which shows seasonally contrasting hypolimnetic oxygen conditions. Larvae stayed in sediment and water bottom during day and ascended to surface during night. Results indicate that feeding activity is limited mainly to the plankton population. Phytoplankton, rotifers or remains of Chaoborus larvae were not found in crops. With the exception of ostracods, all crustacean prey available in the zooplankton occurred in the guts. Ceriodaphnia cornuta and Moina micrura were the most frequent food items (about 75% of occurrence frequency) and were positively selected. The remainder crustacean zooplankton taxa were negatively selected by larvae. The most intense feeding activity in larvae occurred near midnight and sunrise, in dates when the hypolimnion was anoxic. When oxygen was available on the bottom, a higher and not changing diel feeding activity was detected. Our results indicate that vertical migration may promote a spatial separation between larvae and zooplankton, and feeding activity of larvae occurred only when both overlapped. (© 2005 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes

1. Structural complexity may stabilise predator–prey interactions and affect the outcome of trophic cascades by providing prey refuges. In deep lakes, vulnerable zooplankton move vertically to avoid fish predation. In contrast, submerged plants often provide a diel refuge against fish predation for large‐bodied zooplankton in shallow temperate lakes, with consequences for the whole ecosystem. 2. To test the extent to which macrophytes serve as refuges for zooplankton in temperate and subtropical lakes, we introduced artificial plant beds into the littoral area of five pairs of shallow lakes in Uruguay (30°–35°S) and Denmark (55°–57°N). We used plants of different architecture (submerged and free‐floating) along a gradient of turbidity over which the lakes were paired. 3. We found remarkable differences in the structure (taxon‐richness at the genus level, composition and density) of the zooplankton communities in the littoral area between climate zones. Richer communities of larger‐bodied taxa (frequently including Daphnia spp.) occurred in the temperate lakes, whereas small‐bodied taxa characterised the subtropical lakes. More genera and a higher density of benthic/plant‐associated cladocerans also occurred in the temperate lakes. The density of all crustaceans, except calanoid copepods, was significantly higher in the temperate lakes (c. 5.5‐fold higher). 4. Fish and shrimps (genus Palaemonetes) seemed to exert a stronger predation pressure on zooplankton in the plant beds in the subtropical lakes, while the pelagic invertebrate Chaoborus sp. was slightly more abundant than in the temperate lakes. In contrast, plant‐associated predatory macroinvertebrates were eight times more abundant in the temperate than in the subtropical lakes. 5. The artificial submerged plants hosted significantly more cladocerans than the free‐floating plants, which were particularly avoided in the subtropical lakes. Patterns indicating diel horizontal migration were frequently observed for both overall zooplankton density and individual taxa in the temperate, but not the subtropical, lakes. In contrast, patterns of diel vertical migration prevailed for both the overall zooplankton and for most individual taxa in the subtropics, irrespective of water turbidity. 6. Higher fish predation probably shapes the general structure and dynamics of cladoceran communities in the subtropical lakes. Our results support the hypothesis that horizontal migration is less prevalent in the subtropics than in temperate lakes, and that no predator‐avoidance behaviour effectively counteracts predation pressure in the subtropics. Positive effects of aquatic plants on water transparency, via their acting as a refuge for zooplankton, may be generally weak or rare in warm lakes.     

Food and food selection of cisco (Coregonus albula L.) in a dysoligotrophic lake

With minor exceptions, cisco (C. albula) in Lake Suomunjärvi fed on cladocerans and copepods. The food habits were different among two size classes of fish. The composition of cisco diet changed at different depths and times of the day, but the distribution of zooplankton was usually very similar in each period irrespective of the depth or diel period. Daphnia, Bosmina, Cyclops scutifer and Heterocope appendiculata were the main diet of cisco. Calculations of fish electivity indices showed that cisco selected usually large species of cladocerans and copepods and a small cladoceran, Bosmina coregoni. Body-size selection was clear for Daphnia and Bosmina.     

Local genetic adaptation generates latitude‐specific effects of warming on predator–prey interactions

Temperature effects on predator–prey interactions are fundamental to better understand the effects of global warming. Previous studies never considered local adaptation of both predators and prey at different latitudes, and ignored the novel population combinations of the same predator–prey species system that may arise because of northward dispersal. We set up a common garden warming experiment to study predator–prey interactions between Ischnura elegans damselfly predators and Daphnia magna zooplankton prey from three source latitudes spanning >1500 km. Damselfly foraging rates showed thermal plasticity and strong latitudinal differences consistent with adaptation to local time constraints. Relative survival was higher at 24 °C than at 20 °C in southern Daphnia and higher at 20 °C than at 24 °C, in northern Daphnia indicating local thermal adaptation of the Daphnia prey. Yet, this thermal advantage disappeared when they were confronted with the damselfly predators of the same latitude, reflecting also a signal of local thermal adaptation in the damselfly predators. Our results further suggest the invasion success of northward moving predators as well as prey to be latitude‐specific. We advocate the novel common garden experimental approach using predators and prey obtained from natural temperature gradients spanning the predicted temperature increase in the northern populations as a powerful approach to gain mechanistic insights into how community modules will be affected by global warming. It can be used as a space‐for‐time substitution to inform how predator–prey interaction may gradually evolve to long‐term warming.     

The essential omega-3 fatty acid EPA affects expression of genes involved in the metabolism of omega-6-derived eicosanoids in Daphnia magna

We quantified the predation of Acanthocyclops americanus from the shallow Mediterranean lake Albufera, using gut contents from field collections and laboratory feeding tests. For functional response studies, we used Brachionus plicatilis (at 6 concentrations, 400–4000 ind. 40 ml⁻¹) and Diaphanosoma mongolianum (at 2–20 ind. 40 ml⁻¹). Copepod feeding rates were also estimated using different proportions of rotifer prey and lake seston (0–67.5% of seston + 40 individuals of B. plicatilis). Prey selection studies were conducted using five zooplankton species: Brachionus angularis, Brachionus plicatilis, Keratella tropica, Daphnia magna and Diaphanosoma mongolianum. Gut contents of field-collected adult Acanthocyclops contained filamentous algae and cyanobacteria and 16 zooplankton species (Keratella cochlearis, unspined and spined forms, K. tropica, Brachionus plicatilis, Brachionus calyciflorus, Brachionus angularis, Brachionus variabilis, Asplanchna girodi, Polyarthra vulgaris, Synchaeta pectinata, Lepadella rhomboides, unidentified bdelloids, Alona rectangula, Chydorus sphaericus, Bosmina longirostris, D. magna, Ceriodaphnia dubia and copepod nauplii). When fed B. plicatilis or D. mongolianum, female A. americanus had higher prey consumption rates than males. Increased proportion of lake seston caused reduced consumption of brachionid prey. Our data suggest that A. americanus is omnivorous in nature.

     

Predator induced life-history shifts in a freshwater cladoceran

Summary Life-history theory predicts that maturity and resource allocation patterns are highly sensitive to selective predation. Under reduced adult survival, selection will favour genotypes capable of reproducing earlier, at a smaller size and with a higher reproductive effort. When exposed to water that previously held fish, (size selective predators which prefer larger Daphnia), individuals of Daphnia hyalina reproduced earlier, at a smaller size and had a higher reproductive investment. Hence the prey was able to switch its life history pattern in order to become less susceptible to predation by a specific predator. The cue that evokes the prey response is a chemical released by the predator.     

Habitat segregation and interactive effects of multiple predators on a prey assemblage

1. In a field experiment we examined the interactive effects of two common predators of zooplankton, bluegill sunfish (Lepomis macrochirus) and Chaoborus spp. on the growth rate and habitat use of three congeneric prey species (Daphnia). Bluegill and Chaoborus both consume Daphnia, but bluegill also prey on Chaoborus. The prey species, Daphnia pulicaria, D. rosea and D. retrocurva, differed in body size and vertical distribution. We expected the largest species, D. pulicaria, to be most vulnerable to fish predation and the smallest species, D. retrocurva, to be most vulnerable to Chaoborus predation. 2. As we expected, the population growth rate of D. pulicaria was significantly reduced by fish. However, Chaoborus also significantly reduced the growth rate of this species. No significant interaction effect was detected, indicating that the effect of these predators was additive. The growth rates of D. rosea and D. retrocurva were significantly reduced by Chaoborus, but a significant interaction effect indicated that the effect of Chaoborus was stronger in the absence of fish than when fish were present. Therefore the impact of Chaoborus and fish on D. rosea and D. retrocurva was non-additive. The interactive effect of the two predators on D. retrocurva was greater in magnitude than on D. rosea. 3. In the absence of predators, the three Daphnia species showed no differences in mean habitat depth between day and night. Both predators significantly affected diel habitat use of D. pulicaria and D. rosea. Fish caused both of these Daphnia species to move deeper during the day, whereas Chaoborus caused Daphnia to move into shallower water at night. Daphnia retrocurva tended to migrate upwards at night in all predator treatments, but no significant differences in migration were observed among the predator treatments. The effects of predators on habitat use were not interactive for any prey species. 4. Our results suggest that body size, habitat use and the diel migratory response to predators are important factors mediating the interactive effects of multiple predator types on zooplankton.     

Characterizing a zooplankton neighbourhood: small-scale patterns of association and abundance

• 1 This study compares small-scale (i.e. neighbourhood) associations among distributions of phytoplankton, zooplankton, and zooplankton grazing rates using a combination of correlations and analyses of spatial patchiness.
• 2 All zooplankton and phytoplankton populations had patchy distributions. On average, individuals experienced members of their same taxon at a density that was 42% greater than the mean sample density.
• 3 The various zooplankton taxa experienced different average neighbourhoods, even within the same stratum of the lake. For example, Daphnia galeata mendotae (Birge) experienced phytoplankton concentrations that were nearly 50% greater than those experienced by Daphnia pulicaria (Forbes) at the same depth.
• 4 The distributions of the various phytoplankton taxa were positively correlated with each other, but the distributions of zooplankton were negatively correlated, or more often, unrelated to each other.
• 5 Phytoplankton abundance was negatively correlated with zooplankton grazing rates.
• 6 We hypothesize that while phytoplankton distributions are driven by common external factors, the factors that determine horizontal distributions of zooplankton are species specific. In addition, zooplankton grazing appears at least partially responsible for the generation of patchiness in the distribution of phytoplankton.

     

The effects of selective fish predation on the horizontal distribution of pelagic Cladocera in a southern French reservoir

A four-year study showed a clear seasonal succession of species within the cladoceran community of the large, oligotrophic Sainte-Croix reservoir (S.E. France). Diaphanosoma brachyurum and Ceriodaphnia pulchella were strictly limited to the warm stratified period (July to October), whereas Bosmina longirostris and Bosmina coregoni were dominant during spring and autumn. Daphnia longispina was the only species to occur throughout the year with higher densities in spring.In spring and late autumn, the discharge of the inflowing river Verdon was high and the abundance of all species showed a gradient over the whole lake with lower densities close to the inflow. During the stratified period, water inflow was very low and species showed different patterns. Densities of the small form Ceriodaphnia pulchella were similar all along the long axis of the lake, whereas Daphnia densities were significantly higher near the dam. The distribution pattern of Diaphanosoma, an intermediate-sized species, showed similar trends to that of Daphnia. The only planktivorous fish in the pelagic zone, the bleak (Alburnus alburnus), fed mostly on large-bodied species (> 1.0 mm) and was more abundant close to the inflow current. A comparison between the length frequency distributions of cladocera upstream and downstream provided a clear demonstration of the effects of size-selective predation on prey populations. Finally, the interactions between spatial heterogeneity and long-term development of the zooplankton community and the indirect effects of predation are discussed.     

Effect of vertebrate predation on the spatio-temporal distribution of cladocerans in a temperature eutrophic lake

We analysed the spatio-temporal distribution of zooplankton along a profile of 10 stations from the shore to the pelagic zone from April to September 1988, the period when the larvae and juveniles Rutilus rutilus, the most abundant species in the Lake, are in the littoral zone. The digestive tracts of the young roach were analysed. They fed essentially on rotifers and on cladocerans. For comparison, zooplankton was also analysed at one littoral area without fish fry. There was an increase of cladoceran density from the vegetated nearshore zone to the offshore zone. Considering the density of Bosmina longirostris, Daphnia longispina, Chydorus sphaericus and Ceriodaphnia quadrangula, we observed a different distribution pattern in the course of the year. In the nearshore zone, the relative abundance of small species, Bosmina and Chydorus, was much higher than that of the larger Daphnia. From April to September, predation pressure mainly affected the smallest species: in contrast to the inshore station without fish fry, the density of Bosmina decreased in May in the littoral with fish. Chydorus was concentrated in the littoral between February and April, then grew into the pelagic zone, where predation pressure obviously was low during the warm season. The number of Daphnia, which was eaten by the fish fry at any time, remained low in the nearshore zone, which suggests that the presence of fish may cause Daphnia to avoid this zone. Ceriodaphnia which was not affected by this predation, was scarce in the nearshore zone during mid-summer. The low density of the cladocerans in the nearshore zone is likely associated with vertebrate predation by roach fry and juveniles, the result of such a process being either a depletion in density of the prey, or an avoidance behaviour.     

Esteval phenology of an Acanthocyclops (Crustacea,Copepoda) in a Colorado tarn with remarks on the vernalis-robustus complex

Weekly mean lenghts of adult female Acanthocyclops robustus ranged between 1.14 and 1.41 mm in a Colorado alpine lake during the summer of 1966. The smallest animals occurred in late September and the largest in mid-August, corresponding to development in warm and cool water, respectively. The males also declined in mean length during the course of the summer and were about 70% of the length of the females on any date. About 75% of the females possessed a 3.4.4.4 spine formula; 8%, 2.3.3.3 and 17% an anomalous formula. Eight-one percent of the males had a 3.4.4.4 formula; 7%, 2.3.3.3 and 12% were anomalous. Morphological variation, and breeding experiments performed by Price (1958) suggest that A. robustus and A. vernalis as defined by Kiefer (1976) are likely species complexes, rather than just two species.