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USGS1982

Anticholinesterase poisoning of birds: Field monitoring and diagnosis of acute poisoning

Organophosphorus and carbamate pesticides are cholinesterase (ChE) inhibiting chemicals that have been responsible for avian die-offs. Identification of chemicals implicated in these die-offs is difficult and sometimes conclusions are solely circumstantial. However, when marked depression (inhibition) of brain ChE activity accompanies organophosphorus or carbamate residues in body tissues or ingesta, cause-effect diagnosis is enhanced. To achieve this end, normal brain ChE activity is estimated for controls of the affected species and then die-off specimens are individually evaluated for evidence of ChE inhibition. This approach to evaluation of antiChE poisoning may also be used to monitor exposure of vertebrates to field application of organophosphorus or carbamate pesticides. Problems associated with this kind of evaluation, and the main topic of this report, include variability of brain ChE activity among species, postmortem influences of ambient conditions (storage or field) on ChE activity, and differential patterns of ChE activity when inhibited by organophosphorus or carbamate compounds. Other topics discussed are the ChE assay procedure, example case reports and interpretation, and research needed for improving the diagnostic utility of ChE activity in a field situation.

Environmental Toxicology and Chemistry↗

USGS1986

Mortality of captive whooping cranes caused by eastern equine encephalitis virus

Of 39 captive whooping cranes (Grus americana), 7 died during a 7-week period (Sept 17 through Nov 4, 1984) at the Patuxent Wildlife Research Center, Laurel, Md. Before their deaths, 4 cranes did not develop clinical signs, whereas the other 3 cranes were lethargic and ataxic, with high aspartate transaminase, gamma-glutamyl transferase, and lactic acid dehydrogenase activities, and high uric acid concentrations. Necropsies indicated that the birds had ascites, intestinal mucosal discoloration, fat depletion, hepatomegaly, splenomegaly, and visceral gout. Microscopically, extensive necrosis and inflammation were seen in many visceral organs; the CNS was not affected. Eastern equine encephalitis (EEE) virus was isolated from specimens of the livers, kidneys, lungs, brains, and intestines of 4 of the 7 birds that died, and EEE virus-neutralizing antibody was detected in 14 (44%) of the 32 surviving birds. Other infectious or toxic agents were not found. Morbidity or mortality was not detected in 240 sandhill cranes (Grus canadensis) interspersed among the whooping cranes; however, 13 of the 32 sandhill cranes evaluated had EEE virus-neutralizing antibody. Of the 41 wild birds evaluated in the area, 3 (4%) had EEE virus-neutralizing antibody. Immature Culiseta melanura (the most probable mosquito vector) were found in scattered foci 5 km from the research center.

Maryland↗

USGS1991

Acute toxicity of four anticholinesterase insecticides to American kestrels, eastern screech-owls and northern bobwhites

American kestrels (Falco sparverius), eastern screech-owls (Otus asio), and northern bobwhites (Colinus virginianus) were given single acute oral doses of four widely diverse anticholinesterase pesticides: EPN, fenthion, carbofuran, and monocrotophos. LD50s, based on birds that died within 5 d of dosage, were computed for each chemical in each species. Sex differences in the sensitivity of northern bobwhites in reproductive condition were examined. American kestrels were highly sensitive to all chemicals tested (LD50s 0.6--4.0 mg/kg). Eastern screech-owls were highly tolerant to EPN (LD50 274 mg/kg) but sensitive to the remaining chemicals (LD50s 1.5-3.9 mg/kg). Northern bobwhites were highly sensitive to monocrotophos (LD50 0.8 mg/kg) and less sensitive to the remaining chemicals (LD50s 4.6--31 mg/kg). Female bobwhites (LD50 3.1 mg/kg) were more sensitive to fenthion than males (LD50 7.0 mg/kg). Mean percent depression of brain cho[inesterase (ChE) of birds that died on the day of dosing exceeded 65% for all chemicals in all species. The response of one species to a given pesticide should not be used to predict the sensitivity of other species to the same pesticide. The need for research on several topics is discussed

Environmental Toxicology and Chemistry↗

USGS1981

Effects of malathion, diazinon, and parathion on mallard embryo development and cholinesterase activity

The effects of external exposure of mallard ( Anas platyrhynchos ) eggs to malathion, diazinon, and parathion were examined using formulations and concentrations similar to field applications. Treatment with aqueous emulsion simulated exposure at the rate of 100 gal per acre (153 liters/hectare) with three to six different doses per compound with treatment at 3 and 8 days of embryonic development. Treatment with a nontoxic oil vehicle simulated exposure at the rate of 11 gal per acre (16.8 liters/hectare) with three to six different doses per compound. The order of embryotoxicity on a pounds-per-acre basis was parathion > diazinon > malathion with either vehicle. However, the potential hazard under conditions of up to five times the maximum field level of application was greater for malathion because of the high permissible level of application for malathion on certain crops. Parathion, the most embryotoxic of the three, had the most pronounced effects when an oil vehicle was used, as reflected by an LC 50 of about 2 lb of active ingredient per acre, stunted growth, and a high frequency of malformations involving distortion of the axial skeleton, particularly in the cervical region. All three compounds resulted in significant depression of plasma and brain cholinesterase activity, but parathion caused the most depression throughout development, which was still apparent in hatchlings. Treatment with either distilled water or oil vehicle alone did not result in any of these effects seen with organophosphorous insecticides.

Environmental Research↗

USGS2020

Rabies outbreak in captive big brown bats (Eptesicus fuscus) used in white-nose syndrome vaccine trial

An outbreak of rabies occurred in a captive colony of wild-caught big brown bats ( Eptesicus fuscus ). Five of 27 bats exhibited signs of rabies virus infection 22–51 d after capture or 18–22 d after contact with the index case. Rabid bats showed weight loss, aggression, increased vocalization, hypersalivation, and refusal of food. Antigenic typing and virus sequencing confirmed that all five bats were infected with an identical rabies virus variant that circulates in E. fuscus in the United States. Two bats with no signs of rabies virus infection were seropositive for rabies virus-neutralizing antibodies; the brains of these bats had no detectable viral proteins by the direct fluorescence antibody test. We suspect bat-to-bat transmission of rabies virus occurred among our bats because all rabies-infected bats were confined to the cage housing the index case and were infected with viruses having identical sequences of the entire rabies nucleoprotein gene. This outbreak illustrated the risk of rabies virus infection in captive bats and highlights the need for researchers using bats to assume that all wild bats could be infected with rabies virus.

Journal of Wildlife Diseases↗

USGS1981

Gray bats and pollution in Missouri and northern Alabama

Gray bats died with lethal brain concentrations of dieldrin and rising levels of heptachlor epoxide in 1976, 1977, and 1978 at Bat Caves No. 2-3, Franklin County, Missouri. The colony disappeared in 1979. Dieldrin was banned in 1974 and 1981 was the last year for heptachlor use in Missouri. The State is recommendiing three organophosphates (chlorpyrifos or Dursban, dyfonate or Fonophos, and ethoprop or Mocap) as substitutes for heptachlor. All three compounds have excellent records in the environment. Analyses of insects collected where bats of this colony fed showed beetles, particularly rove beetles (Staphylinidae), to be the most heavily contaminated part of the bat's diet. Lactation concentrated these residues so that levels in milk were approximately 30 times those in the insect diet. Gray bats found dead in caves in northern Alabama showed DDD (a DDT derivative) contamination. Bats from the colony at Cave Springs Cave on the Wheeler National Wildlife Refuge contained up to 29 ppm DDD in their brains, but this is probably less than one-half the lethal level. Bats from other colonies contained less. The DDD contamination enters the Terinessee River just above the Wheeler Refuge and is seen in gray bat colonies as far as 60 miles downriver.

Bat Research News↗

USGS2012

Arsenic-induced biochemical and genotoxic effects and distribution in tissues of Sprague-Dawley rats

Arsenic (As) is a well documented human carcinogen. However, its mechanisms of toxic action and carcinogenic potential in animals have not been conclusive. In this research, we investigated the biochemical and genotoxic effects of As and studied its distribution in selected tissues of Sprague–Dawley rats. Four groups of six male rats, each weighing approximately 60 ± 2 g, were injected intraperitoneally, once a day for 5 days with doses of 5, 10, 15, 20 mg/kg BW of arsenic trioxide. A control group was also made of 6 animals injected with distilled water. Following anaesthetization, blood was collected and enzyme analysis was performed by spectrophotometry following standard protocols. At the end of experimentation, the animals were sacrificed, and the lung, liver, brain and kidney were collected 24 h after the fifth day treatment. Chromosome and micronuclei preparation was obtained from bone marrow cells. Arsenic exposure significantly increased ( p < 0.05) the activities of plasma alanine aminotransferase–glutamate pyruvate transaminase (ALT/GPT), and aspartate aminotransferase–glutamate oxaloacetate transaminase (AST/GOT), as well as the number of structural chromosomal aberrations (SCA) and frequency of micronuclei (MN) in the bone marrow cells. In contrast, the mitotic index in these cells was significantly reduced ( p < 0.05). These findings indicate that aminotransferases are candidate biomarkers for arsenic-induced hepatotoxicity. Our results also demonstrate that As has a strong genotoxic potential, as measured by the bone marrow SCA and MN tests in Sprague–Dawley rats. Total arsenic concentrations in tissues were measured by inductively coupled plasma mass spectrometry (ICP-MS). A dynamic reaction cell (DRC) with hydrogen gas was used to eliminate the ArCl interference at mass 75, in the measurement of total As. Total As doses in tissues tended to correlate with specific exposure levels.

Microchemical Journal↗

USGS2017

Uptake and disposition of select pharmaceuticals by bluegill exposed at constant concentrations in a flow-through aquatic exposure system

The increasing use of pharmaceuticals has led to their subsequent input into and release from wastewater treatment plants, with corresponding discharge into surface waters that may subsequently exert adverse effects upon aquatic organisms. Although the distribution of pharmaceuticals in surface water has been extensively studied, the details of uptake, internal distribution, and kinetic processing of pharmaceuticals in exposed fish have received less attention. For this research, we investigated the uptake, disposition, and toxicokinetics of five pharmaceuticals (diclofenac, methocarbamol, rosuvastatin, sulfamethoxazole, and temazepam) in bluegill sunfish ( Lepomis macrochirus ) exposed to environmentally relevant concentrations (1000–4000 ng L –1 ) in a flow-through exposure system. Temazepam and methocarbamol were consistently detected in bluegill biological samples with the highest concentrations in bile of 4, 940, and 180 ng g –1 , respectively, while sulfamethoxazole, diclofenac, and rosuvastatin were only infrequently detected. Over 30-day exposures, the relative magnitude of mean concentrations of temazepam and methocarbamol in biological samples generally followed the order: bile ≫ gut > liver and brain > muscle, plasma, and gill. Ranges of bioconcentration factors (BCFs) in different biological samples were 0.71–3960 and 0.13–48.6 for temazepam and methocarbamol, respectively. Log BCFs were statistically positively correlated to pH adjusted log K ow (that is, log D ow ), with the strongest relations for liver and brain ( r 2 = 0.92 and 0.99, respectively), implying that bioconcentration patterns of ionizable pharmaceuticals depend on molecular status, that is, whether a pharmaceutical is un-ionized or ionized at ambient tissue pH. Methocarbamol and temazepam underwent rapid uptake and elimination in bluegill biological compartments with uptake rate constants ( K u ) and elimination rate constants ( K e ) at 0.0066–0.0330 h –1 and 0.0075–0.0384 h –1 , respectively, and half-lives at 18.1–92.4 h. Exposure to mixtures of diclofenac, methocarbamol, sulfamethoxazole, and temazepam had little or no influence on the uptake and elimination rates, suggesting independent multiple uptake and disposition behaviors of pharmaceuticals by fish would occur when exposed to effluent-influenced surface waters.

Environmental Science & Technology↗

USGS1968

Electrophoretic separation of fish brain esterases

Fish brains were homogenized in an all-glass Potter-Elvehjem-type tissue grinder in 40% sucrose solution. The homogenate concentration was 10 brains/ml for both the bluegill and channel catfish. The brei was centrifuged at 34,700 g for 30 min at 5 C, and 30 J.lliters of the supernatant were used per column for electrophoresis.

Journal of the Fisheries Research Board of Canada↗

USGS1998

Organochlorines, mercury, and selenium in great blue heron eggs from Indiana Dunes National Lakeshore, Indiana

In 1993, 20 great blue heron (Ardea herodias; GBH) eggs (one per nest) were collected from a colony at the Indiana Dunes National Lakeshore, Indiana (INDU). The eggs were artificially incubated until pipping and were then analyzed for organochlorines, mercury, and selenium. Livers of embryos were analyzed for hepatic microsomal ethoxyresorufin-O-dealkylase (EROD) activity. Brains were measured for asymmetry. Egg-laying began in early April and the mean clutch size was 4.2 eggs per clutch. Organochlorine concentrations were generally low (geometric mean p,p’-DDE = 1.6 /μg/g wet weight; polychlorinated biphenyl [PCB] = 4.9 μg/g); however, one egg had elevated concentrations of p,p -DDE (13 /μg/g) and PCBs (56 /μg/g). EROD activity in the embryos analyzed from INDU was not elevated. The frequency (11%) of brain asymmetry was low. Eggshells averaged 3.4% thinner than eggshells collected prior to the use of DDT. Mercury (geometric mean = 0.9 μg/g dry weight) concentrations in GBH eggs were within background levels. Selenium (4.0 μg/g dry weight) concentrations in eggs were above background levels, but below a concentration threshold associated with reproductive impairment.

Journal of Great Lakes Research↗

USGS1984

Heptachlor seed treatment contaminates hawks, owls, and eagles of Columbia Basin, Oregon

We evaluated organochlorine residues in 12 species of hawks. owls, and eagles from the Columbia Basin of Oregon between 1978 and 1981. Companion studies showed that heptachlor epoxide (HE) induced adult mortality and reduced productivity of the Canada Goose (Branta canadensis) and American Kestrel (Falco sparverius).ln this study, brain tissue from raptors found dead and sample eggs from 90 nests were analyzed for organochlorines. The primary concern was HE that entered raptor food chains through the ingestion of heptachlor-treated seed by their prey. HE residues were detected in eggs from 9 of 10 species and ranged as high as 4.75 ppm (wet wt), but no definite effects of HE on productivity were readily apparent from the limited series of nests. However, the hazard of heptachlor seed treatments to birds of prey was demonstrated by the occurrence of lethal residues of HE in brain tissue of 3 Golden Eagles (Aquila chrysaetos) and 1 Rough-legged Hawk (Buteo lagopus). Other organochlorine pesticides were present in the eggs and significant relationships were found between DDE and eggshell thickness for the Swainson's Hawk (Buteo swainsoni) and Western Screech-Owl (Otus kennicotti), although shell thinning (9.6% and 7.4%) was below the generally accepted range where reproductive problems have been known to occur.

Raptor Research↗

USGS2004

Rabies in a captive colony of big brown bats (Eptesicus fuscus)

Our research has focused on the ecology of commensal populations of big brown bats ( Eptesicus fuscus ) in Fort Collins, Colorado (USA), in relation to rabies virus (RV) transmission. We captured 35 big brown bats ( Eptesicus fuscus ) in late summer 2001 and held them captive for 4.8 mo. The bats were initially placed in an indoor cage for 1 mo then segregated into groups of two to six per cage. Two of the bats succumbed to rabies virus (RV) within the first month of capture. Despite group housing, all of the remaining bats were healthy over the course of the investigation; none developed rabies, although one of the rabid bats was observed to bite her cage mates. Reverse transcription–polymerase chain reaction (RT-PCR) and Taqman ® real-time PCR analysis of the RNA derived from the brain tissue, salivary glands, and oral swab samples confirmed RV infection in the dead bats. Rabies virus was also isolated from the brain tissue upon passage in mouse neuroblastoma cells. Nucleotide sequence analysis of the RV nucleoprotein (N) gene showed 100% identity with the N gene sequence of a 1985 E. fuscus isolate from El Paso County, Colorado. Bat sera obtained six times throughout the study were assayed for RV neutralizing antibodies using the rapid fluorescent focus inhibition test. The RV neutralizing activity in the serum was associated with the IgG component, which was purified by binding to protein G Sepharose. Five bats were RV seropositive prior to their capture and maintained titers throughout captivity. Two adult bats seroconverted during captivity. Two volant juvenile bats had detectable RV antibody titers at the first serum collection but were negative thereafter. Four seronegative bats responded to a RV vaccine administration with high titers of RV antibodies. A serologic survey of big brown bats in the roost from which one of the captive rabid bats had originated showed a significant rise in seroprevalence during 2002.

Journal of Wildlife Diseases↗

USGS1968

Some enzymatic properties of brain Acetylcholinesterase from bluegill and channel catfish

Using a manometric technique an acetylcholinesterase (EC 3.1.1.7, acetylcholine acetyl-hydrolase) was demonstrated in brain tissue from the bluegill, Lepomis macrochirus Rafinesque, and the channel catfish, Ictalurus punctatus (Walbaum). The activities were 19 and 37&ensp;μmoles acetylcholine hydrolyzed/milligram protein per hour for the bluegill and channel catfish enzymes, respectively. The optimum substrate concentration for the hydrolysis of acetylcholine was 10&ensp;m M for the enzymes from both species. Generally, the catfish acetylcholinesterase was somewhat more susceptible than the bluegill to the inhibitors tested; however, the bluegill enzyme was more susceptible to inhibition by malathion and malaoxon.

Journal of the Fisheries Research Board of Canada↗

USGS1981

An evaluation of blood plasma for monitoring DDE in birds of prey

Laboratory and field studies show that DDE residues in blood plasma are highly correlated with DDE in the brain, the rate of DDE exposure and the amount of DDE in eggs of free-living birds of prey. A blood sampling approach is proposed to supplement existing environmental contaminant methods available for birds of prey. Residues (ΣDDT) in plasma provide some direct information; however, a method is proposed to adjust blood plasma residues from four species of birds of prey to the estimated residues in eggs for the purpose of residue interpretation. The blood plasma-egg relationship appears to be species-independent in the four raptors studied. Two predicting equations are presented for estimating egg residues, one for plasma samples collected prior to, or within a few days of, egg laying, and another for the post-laying period. Limitations and advantages of the blood plasma monitoring approach are discussed. The approach may be particularly suitable for endangered species research.

Environmental Pollution (Series A)↗

USGS2009

Pathogenicity of West Nile virus and response to vaccination in sandhill cranes ( Grus canadensis ) using a killed vaccine

West Nile virus was introduced into the United States in the vicinity of New York, New York, USA in 1999. The virus has since killed large numbers of birds nationwide, especially, but not limited to, crows ( Corvus brachyrhinchos ). One sandhill crane ( Grus canadensis ) at the Bridgeport Zoo (Bridgeport, Connecticut, USA) reportedly died from West Nile virus, so sandhill cranes and endangered whooping cranes ( Grus americana ), both in the wild and in captive breeding colonies at United States Geological Service (USGS) Patuxent Wildlife Research Center (Laurel, Maryland, USA) were considered at risk. A killed vaccine in sandhill cranes was evaluated by vaccinating and then challenging these cranes with live West Nile virus. No sandhill cranes inoculated with the killed vaccine developed significant titers when compared with unvaccinated controls. No sandhill cranes inoculated with the vaccine and challenged with the virus died from West Nile virus infection. In addition, no unvaccinated challenged sandhill cranes died. However, 2 days postchallenge, vaccinated cranes had significantly less viremia (P < 0.05) than unvaccinated cranes. Seven days postchallenge vaccinated cranes had significantly less cloacal shedding of the virus (P < 0.05) than unvaccinated cranes and significantly less weight loss (P < 0.05) as compared with unvaccinated cranes. Vaccinated sandhill cranes developed significantly higher titers 14 days postchallenge and were viremic for shorter periods of time after challenge than unvaccinated individuals. Unvaccinated challenged cranes had glial cell aggregates in both the brain and brain stem areas, and this was not observed in vaccinated challenged cranes or in vaccinated unchallenged cranes.

Journal of Zoo and Wildlife Medicine↗

USGS1974

Residues of DDT in lake trout (Salvelinus namaycush) and coho salmon (Oncorhynchus kisutch) from the Great Lakes

Concentrations of DDT residues were higher in lake trout ( Salvelinus namaycush ) from southern Lake Michigan in 1966–70 (average 18.1&ensp;ppm in fish 558–684&ensp;mm long) than in lake trout of the same size-class from Lake Superior in 1968–69 (4.4&ensp;ppm), and higher in adult coho salmon ( Oncorhynchus kisutch ) from Lake Michigan in 1968–71 (averages for different year-classes, 9.9–14.0&ensp;ppm) than in those from Lake Erie in 1969 (2.2&ensp;ppm). Residues were significantly higher in lake trout from southern Lake Michigan than in those from the northern part of the lake. In lakes Michigan and Superior, the levels increased with length of fish and percentage oil. In Lake Michigan coho salmon, the residues remained nearly stable (2–4&ensp;ppm) from September of the 1st yr of lake residence through May or early June of the 2nd yr, but increased three to four times in the next 3&ensp;mo. Residues in Lake Erie coho salmon did not increase during this period, which preceded the spawning season. Although the concentrations of total residues in whole, maturing Lake Michigan coho salmon remained unchanged from August 1968 until near the end of the spawning season in January 1969, the residues were redistributed in the tissues of the spawning-run fish; concentrations in the loin and brain were markedly higher in January than in August. This relocation of DDT residues accompanied a marked decrease in the percentage of oil in the fish, from 13.2 in August to 2.8 in January. Concentrations of residues were relatively high in eggs of both lake trout (4.6&ensp;ppm) and coho salmon (7.4–10.2&ensp;ppm) from Lake Michigan. The percentage composition of the residues ( p , p ′DDE, o , p ′/DDT, p , p ′DDT, and p , p ′DDT) did not differ significantly with life stage, size, age, or locality, or date of collection of lake trout or coho salmon.

Journal of the Fisheries Research Board of Canada↗

USGS2015

Ocean circulation and biogeochemistry moderate interannual and decadal surface water pH changes in the Sargasso Sea

The oceans absorb anthropogenic CO 2 from the atmosphere, lowering surface ocean pH, a concern for calcifying marine organisms. The impact of ocean acidification is challenging to predict as each species appears to respond differently and because our knowledge of natural changes to ocean pH is limited in both time and space. Here we reconstruct 222 years of biennial seawater pH variability in the Sargasso Sea from a brain coral, Diploria labyrinthiformis . Using hydrographic data from the Bermuda Atlantic Time-series Study and the coral-derived pH record, we are able to differentiate pH changes due to surface temperature versus those from ocean circulation and biogeochemical changes. We find that ocean pH does not simply reflect atmospheric CO 2 trends but rather that circulation/biogeochemical changes account for >90% of pH variability in the Sargasso Sea and more variability in the last century than would be predicted from anthropogenic uptake of CO 2 alone.

Geophysical Research Letters↗

USGS1968

Collecting and rearing black flies

This paper, based on a study carried out at the Seney National Wildlife Refuge, Seney, Michigan, and the Patuxent Wildlife Research Center, Laurel, Maryland, describes methods and techniques for collecting, storing, and rearing 8 species of Simuliidae. Included in the study were Cnephia dacotensis (Dyar & Shannon), C. mutata (Malloch), Prosimulium fuscum Syme & Davies, Simulium aureum Fries, S. decorum (Walker), S. venustum Say, S. verecundum Stone & Jamnback, and S. vittattum Zetterstedt. Simuliid eggs collected from a variety of habitats, packed with wet materials in plastic bags and held at 4°C, have remained viable, thus far, up to 424 days. Eggs held at 0° to −70°C failed to hatch when placed in rearing aquariums. Air-dried eggs held at 4°C for 339–535 days failed to hatch after being held in aquariums for 166 days. Immature stages of black flies were successfully reared in 1¼-gallon Pyrex jars and 15-gallon plexiglas aquariums in which the water was agitated by compressed air and aquarium pumps. Water velocities of 0.250–0.542 feet per second were obtained in streams of air bubbles created by use of air stones. Of 21 larval diets used, one consisting of Purina Dog Chow (60-mesh or finer), brain-heart infusion broth, and brewer's yeast powder, and a second consisting of Wayne's dog chow (60-mesh or finer) and brain-heart infusion broth without brewer's yeast powder, were most satisfactory. Larvae were fed 1 gram of diet per 1¼- gallon aquarium and 2 grams per 15-gallon aquarium biweekly. In most of the 225 cultures of S. aureum, S. decorum, S. verecundum, S. venustum, and S. Vittatum it took from 1 to 5 days for the development of eggs to larvae (165 cultures, 73%) and the same number of days for the development of pupae to adults (172 cultures, 76%). Development time for larvae to pupae was fairly closely divided between 11–15 days (63 cultures, 28%) and 16–20 days (53 cultures, 23.6%). The entire period for development from egg to adult after placement of eggs in rearing aquariums was from 21 to 25 days for 26.7% of the cultures.

Annals of the Entomological Society of America↗