Lipid and water depletion in migrating passerines following passage over the Gulf of Mexico

Lipid depletion is currently believed to be the primary factor limiting flight duration of migrating birds in North America, while the influence of water loss is thought to be small. Three migrating species of passerines, wood thrush (Hylocichla mustelina), Swainson's thrush (Catharus ustulatus), and summer tanager (Piranga rubra) were captured during the 1993 spring migration just after crossing the Gulf of Mexico and examined for lipid and water depletion. The redwinged blackbird (Agelaius phoeniceus), a winter resident, was examined for comparison. Although some migrants had low levels of fat, most were not seriously fat-depleted and had much higher lipid levels than red-winged blackbirds. Migrants appeared dehydrated, usually having less than 60% body water and significantly less water than the blackbirds. Recaptured wood thrushes had significantly higher mass than when initially captured. Many of these birds were replenishing significant amounts of water, while the acquisition of lipid mass was dependent on the amount of time the birds spent on the study site. Migrants were significantly fatter but had significantly less water mass when captured during unfavorable weather than under favorable conditions. It appears that both dehydration and lipid depletion are major physiological constraints on migrating passerines.     

Avian Community Structure Along a Mountain Big Sagebrush Successional Gradient

Abstract: We compared vegetative structure and bird communities among 4 successional states in central Oregon representing a continuum from 1) postburn grassland, 2) mountain big sagebrush—Idaho fescue (Artemisia tridentatA—Festuca idahoensis) shrub—steppe, 3) sagebrush—steppe—juniper (Juniperus occidentalis), to 4) old-growth western juniper. Species richness, evenness, and diversity of bird communities were highest in old-growth and mid-successional juniper (22.9 species/transect and 23.6 species/transect, respectively) but lowest in the grasslands (17.6 species/transect). Bird species diversity was positively correlated with physiognomic cover diversity (r = 0.74, P = 0.001). Density of breeding birds was greatest in old-growth juniper (6.6 birds/ha) and lowest in postburn grasslands (3.6 birds/ha) but similar in shrub—steppe and sagebrush—steppe—juniper (6.0 birds/ha and 5.5 birds/ha, respectively). Old-growth juniper had the highest total densities of both tree and cavity nesters. Mountain chickadees (Parus gambeli), Cassin's finches (Carpodacus cassinii), chipping sparrows (Spizella passerina), brown-headed cowbirds (Molothrus ater), mountain bluebirds (Sialia currucoides), dark-eyed juncos (Junco hyemalis), Empidonax flycatchers, ash-throated flycatchers (Myiarchus cinerascens), and northern flickers (Colaptes auratus) were more abundant in cover types dominated by junipers. Vesper sparrows (Pooecetes gramineus), western meadowlarks (Sturnella neglecta), green-tailed towhees (Pipilo chlorurus), and horned larks (Eremophila alpestris) were associated with grassland communities. Brewer's sparrows (Spizella breweri), sage sparrows (Amphispiza belli), sage thrashers (Oreoscoptes montanus), and horned larks (Eremophila alpestris) were most abundant in sagebrush cover types. Management strategies should restore or maintain the desired proportions of the different successional states to maintain populations of grassland and sagebrush birds while providing habitat for tree and cavity nesting species.     

Environmental,geographical and time-related impacts on avian malaria infections in native and introduced populations of house sparrows (Passer domesticus), a globally invasive species

Aim

The increasing spread of vector-borne diseases has resulted in severe health concerns for humans, domestic animals and wildlife, with changes in land use and the introduction of invasive species being among the main possible causes for this increase. We explored several ecological drivers potentially affecting the local prevalence and richness of avian malaria parasite lineages in native and introduced house sparrows (Passer domesticus) populations.

Location

Global.

Time period

2002–2019.

Major taxa studied

Avian Plasmodium parasites in house sparrows.

Methods

We analysed data from 2,220 samples from 69 localities across all continents, except Antarctica. The influence of environment (urbanization index and human density), geography (altitude, latitude, hemisphere) and time (bird breeding season and years since introduction) were analysed using generalized additive mixed models (GAMMs) and random forests.

Results

Overall, 670 sparrows (30.2%) were infected with 22 Plasmodium lineages. In native populations, parasite prevalence was positively related to urbanization index, with the highest prevalence values in areas with intermediate urbanization levels. Likewise, in introduced populations, prevalence was positively associated with urbanization index; however, higher infection occurred in areas with either extreme high or low levels of urbanization. In introduced populations, the number of parasite lineages increased with altitude and with the years elapsed since the establishment of sparrows in a new locality. Here, after a decline in the number of parasite lineages in the first 30 years, an increase from 40 years onwards was detected.

Main conclusions

Urbanization was related to parasite prevalence in both native and introduced bird populations. In invaded areas, altitude and time since bird introduction were related to the number of Plasmodium lineages found to be infecting sparrows.     

The Effect of Hemosporidian Infections on White-Crowned Sparrow Singing Behavior

Relatively little is known about the effects of specific parasites on sexually selected behavioral traits. We subjected free‐living mountain white‐crowned sparrows (Zonotrichia leucophrys oriantha) to a playback experiment to identify the effect of hemosporidian parasites on potentially sexually selected song characteristics. We recorded song after a playback of a novel white‐crowned sparrow song, meant to simulate a territorial intrusion. Infections with Leucocytozoon or Plasmodium influenced singing behavior, while infection with Haemoproteus had no detectable effect. Specifically, song consistency, as measured using a spectrogram correlation, was influenced by both Plasmodium and Leucocytozoon infection. Additionally, birds infected with Plasmodium sang fewer songs following experimental playback. Thus, relatively widespread parasites, like Plasmodium, may have a strong effect on potentially sexually selected song characteristics.     

The post-ovulatory follicles of blackbirds (Agelaius)

Post-ovulatory follicles of tricolored blackbirds (Agelaius tricolor) and redwinged blackbirds (A. phoeniceus) regress from 6.0 to 3.0 mm in length by two days after ovulation and remain less than 3.0 mm during incubation. The follicles of females feeding young average less than 1.0 mm. Serial sections of ovaries of birds in all stages of the nesting cycle show distinct post-ovulatory follicles up to 25 days after ovulation. Lymphocytes, granular polymorphonuclear leucocytes, macrophages, and fibroblasts invade the sloughed granulosa and the hemorrhaged theca interna after ovulation. Granulosa cells, epithelioid cells in the theca interna, and connective tissue cells in the theca externa are lipoidal and cholesterol-positive for at least ten days after ovulation. The rapid regression and histological evidence of degenerating tissue and the invasion of cell types characteristic of the inflammatory response suggest that the ovulated follicles are degenerating rather than secretory organs.     

Response of grassland birds to management in national battlefield parks

Grassland birds are in steep decline, with population declines reported in 74% of North American grassland species in the past 50 years. Declines are particularly severe in the eastern United States where they are influenced by habitat loss and alteration due to urbanization, forest regrowth, and agricultural intensification. The United States National Park Service maintains civil war battlefields in the eastern United States as historical and cultural parks that may also provide habitat refuge for grassland birds within an increasingly urbanized matrix. To assess the conservation importance of battlefield parks and the role of park management in sustaining grassland birds, we surveyed for 2 declining grassland-breeding species, eastern meadowlark (Sturnella magna) and grasshopper sparrow (Ammodramus savannarum), at 242 points across 4 battlefield parks in Maryland, Virginia, and West Virginia, USA, from 2014–2019 and in 2021. We modeled the effects of park management activities (prescribed fire, agricultural leases, and delayed harvest) and habitat and landscape characteristics on breeding-season occupancy. There was support for the influence of local habitat features, landscape, and management. Breeding-season occupancy of both species was consistently higher in hayfields and pasture than in row crops, and both species responded positively to hay and crop harvest delays intended for grassland bird conservation. Prescribed fire within the past 2 years had a positive effect on occupancy of grasshopper sparrows but did not influence eastern meadowlarks. Eastern meadowlarks responded to land cover at multiple spatial scales that are influenced by land use within and outside the parks. Management activities that maintain the parks' cultural goals, including partnerships between national parks and private agricultural operators, are likely to provide valuable habitat for these 2 obligate grassland birds.     

Isospora as an Extraintestinal Parasite of Passerine Birds1

Toxoplasma-like avian parasites inhabiting mononuclear phagocytes have been called Haemogregarina, Toxoplasma. avian Toxoplasma, Atoxoplasma, and Lankesterella by various authors. My attempts to transmit the parasites by bloodsucking mites or by transfer of blood and tissues of infected sparrows and canaries were unsuccessful. However, it was noted that the infection was exacerbated under conditions that favored transmission of coccidiosis: crowding and lack of cleanliness. Oral inoculation of sporulated oocysts of Isospora resulted in death from overwhelming macrophage infection with Toxoplasma-like organisms. Experiments using sparrows and canaries showed that the Isospora species involved was not cross infectious. Further investigations using canaries demonstrated that after oral oocyst inoculation, infection of macrophages spread from the submucosa of the duodenum to the liver. spleen, and lungs. After several generations in the internal organs, asexual multiplication, occured in the intestinal epithelium of the small intestinc. Fecal oocysts first appeared at the end of 9–10 days. Oocysts continued to be passed in the feces for months after infection. This chronicity may be explained by the relatively long life of the macrophages that serve as host cells for the asexual stages as compared to the intestinal epithelium which is the cell type parasitized by conventional coccidia.     

Blood Protozoa of Wild Turkeys in Florida*

From 1969 through 1972, 605 wild turkeys (Meleagris gallopavo Linnaeus) from 10 localities in Florida were examined for blood protozoans. The prevalence in turkeys more than a month old was 84% for Haemoproteus meleagridis Levine, 1961 and 72% for Leucocytozoon smithi Laveran and Lucet, 1905. Sixty-three percent of the birds were infected by both parasites. Infections were most prevalent in juveniles 8–12 months of age. No infection of H. meleagridis or L. smithi was found in 111 poults younger than 35 days. Prevalences were similar in both sexes. Haemoproteus meleagridis was more prevalent (87%) in the southern part of the state; L. smithi was more prevalent (75%) in the north. The prevalence of H. meleagridis did not change during the 4 year period, but L. smithi decreased markedly in 1971, a year of low rainfall. None of the 605 blood films was positive for Plasmodium, but 24 (75%) of 32 blood samples were found by subinoculation technics to be positive for a species of Plasmodium morphologically similar to P. durae Herman, 1941. No trypanosomes were seen on the 605 blood films or in bone marrow cultures (saline-neopeptone-blood) made from 11 turkeys.     

Sexual selection and the geography of Plasmodium infection in Savannah sparrows (Passerculus sandwichensis)

According to Hamilton and Zuk's hypothesis of parasite-mediated sexual selection, host-parasite coevolution maintains variation in male genetic quality and allows for strong intersexual selection in species with high rates of infection. In birds, most interspecific tests of this hypothesis relate the prevalence of blood parasites to some measure of the intensity of sexual selection. Such tests often rely on limited sampling of single populations to estimate species-wide infection rates, and many tests are thus vulnerable to intraspecific (geographic) variation in the evolutionary ecology of disease. Here, we used molecular techniques to examine variation in the prevalence of Plasmodium spp. across 14 populations of Savannah sparrows, Passerculus sandwichensis, in eastern North America. Plasmodium could not be detected in any of 68 island birds, but 34 of 119 (29%) mainland males, and 7 of 43 (16%) mainland females were infected. Among mainland birds, infection was common in southern populations but rare in New Brunswick, Canada. Overall, the prevalence of Plasmodium ranged from 0 to 60% across populations, although only 17.8% of birds were infected in the pooled (species-wide) sample. The extent of this geographic variation suggests that limited sampling of single populations is unlikely to yield accurate estimates of species-wide infection rates. However, among mainland Savannah sparrows, the prevalence of malaria correlated strongly with average male size and the degree of sexual size dimorphism. We speculate that either sexual selection leads to male-biased infection or, conversely, that high rates of infection promote the evolution of strong intersexual selection.     

Variable effects of climate change on six species of North American birds

Many recent studies have shown that birds are advancing their laying date in response to long-term increases in spring temperatures. These studies have been conducted primarily in Europe and at local scales. If climate change is a large-scale phenomenon, then we should see responses at larger scales and in other regions. We examined the effects of long-term temperature change on the laying dates and clutch sizes of six ecologically diverse species of North American birds using 50 years of nest record data. As predicted, laying dates for most (four of six) species were earlier when spring temperatures were warmer. Over the long-term, laying dates advanced over time for two species (red-winged blackbirds, Agelaius phoeniceus and eastern bluebirds, Sialia sialis). Laying date of song sparrows (Melospiza melodia) also advanced with increasing temperature when the analysis was restricted to eastern populations. Neither laying date nor clutch sizes changed significantly over time in the remaining species (American coot, Fulica americana, killdeer, Charadrius vociferous, and American robin, Turdus migratorius), an unsurprising result given the lack of increase in temperatures over time at nest locations of these species. This study indicates that the relationship between climate change and breeding in birds is variable within and among species. In large-scale analyses of North American birds, four of seven species have shown advances in laying dates with increasing temperature (including song sparrows in the east). These variable responses within and among species highlight the need for more detailed studies across large spatial scales.     

Haematozoa of East African birds: III. Three years' observations on the blood parasites of birds from Ngulia

A survey of blood parasites of birds from Ngulia in Kenya was carried out during the period November-December for the years 1973–1975. A total of 468 birds was examined of which 179 (38.2%) were infected with one or more parasites. Together with a re-examination of material from previous surveys for taxonomic purposes, the following species were identified; Haemoproteus anthi, H. centropi, H. columbae, H. coraciae, H. fallisi, H. fringillae, H. lanii, H. morneti, H. orizivorae, H. sanguinis, H. tendeiroi, H. zosteropsi, Leucocytozoon brimonti, L. coccyzus, L. dinizi, L. dub-reuili, L. eurystomi, L. fringillinarum, L. marchouxi, Plasmodium relictum, P. rouxi, P. vaughani, Trypanosoma everetti, T. mayae, T. pycnonoti and Babesiu rustica. Unidentified species of haemogregarines, Aegyptianella, Rickettsia and microfilaria were also observed. The significance of migrant birds as reservoirs of infection, together with the probable seasonality of patent infections in the resident population is discussed.     

Trapping initiates stress response in breeding and non-breeding house sparrows Passer domesticus: implications for using unmonitored traps in field studies

In response to a variety of unpredictable conditions, birds secrete the steroid hormone corticosterone, which has numerous effects on physiology and behavior. A standardized protocol of handling and restraint has been demonstrated to elicit a robust corticosterone response in many species of birds. In contrast, comparatively little is known about the effects of capture technique on corticosterone secretion in wild birds. Setting up multiple live traps checked at regular intervals allows field researchers to capture many birds in a short period of time. However, one potential drawback of this technique is that birds may spend unknown lengths of time in traps prior to sampling. Many birds appear to remain calm and/or feed during this period, potentially leading researchers to assume that corticosterone secretion is unaffected by trapping. We assessed the impact of being left in traps for up to 30 minutes on baseline corticosterone and subsequent corticosterone responses to restraint in non‐breeding and breeding house sparrows Passer domesticus. Traps were baited with seed, and birds were either removed immediately after entry (controls), or left in the trap undisturbed for 15 or 30 min. Upon removal, birds were subjected to a standardized handling/restraint protocol in which blood samples were collected within 3 min, and again at regular intervals for 60 min. Analysis of blood samples revealed that both non‐breeding and breeding sparrows that were held in the traps had significantly higher baseline corticosterone than controls, and showed no further increase in corticosterone secretion in response to handling. However, corticosterone responses to trapping differed seasonally. Our study indicates that although birds did not exhibit prolonged escape behavior while trapped, entry into a walk‐in trap initiated a robust stress response. Taken together with data from a previous study, our data suggest that ornithologists should consider species‐specific and stage‐specific effects of trapping on physiology when designing field studies.     

Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds

The effects of avian malaria parasites of the genus Plasmodium on their hosts are insufficiently understood. This is particularly true for malarial co-infections, which predominant in many bird populations. We investigated effects of primary co-infection of Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (GRW2) on experimentally infected naive juveniles of siskin Spinus spinus, crossbill Loxia curvirostra and starling Sturnus vulgaris. All siskins and crossbills were susceptible but starlings resistant to both these infections. A general pattern of the co-infections was that heavy parasitemia (over 35% during peaks) of both parasites developed in both susceptible host species. There were no significant effects of the co-infections on mean body mass of the majority of infected birds. Mean haematocrit value decreased approximately 1.5 and 3 times in siskins and crossbills at the peak of parasitemia, respectively. Mortality was recorded among infected crossbills. We conclude that co-infections of P. relictum and P. ashfordi are highly virulent and act synergetically during primary infections in some but not all passerine birds.     

Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii amakihi

Six of seven Hawaii Amakihi (Hemignathus virens) with chronic malarial infections had no increases in peripheral parasitemia, declines in food consumption, or loss of body weight when rechallenged with the homologous isolate of Plasmodium relictum 61 to 62 days after initial infection. Five uninfected control amakihi exposed at the same time to infective mosquito bites developed acute infections with high parasitemias. Reductions in food consumption and loss of body weight occurred in all control birds and three of these individuals eventually died. When surviving birds were rechallenged >2 yr later with either the same parasite isolate or an isolate of P. relictum collected on the island of Kauai, all individuals were immune to superinfection. Chronically infected birds developed antibodies to a common suite of malarial antigens ranging in size from 22 to 170 kDa that were detectable as early as 8 days post infection on immunoblots of SDS-polyacrylamide gels. Antibodies to this suite of malarial antigens persisted as long as 1,248 days after initial infection and were consistently detectable at times when parasites were not easily found by microscopy on Giemsa-stained blood smears. The immunoblotting method that is described here appears to be an effective technique for identifying birds with chronic, low-intensity malarial infections when circulating parasites are not easily detectable by microscopy. Hawaiian honeycreepers that are capable of recovering from acute infections develop concomitant immunity to superinfection, making them functionally immune in areas where malaria transmission has become endemic.     

Patterns of haemosporidian prevalence along a range expansion in introduced Kenyan house sparrows Passer domesticus

Avian haemosporidian infections (of the genera Haemoproteus, Plasmodium and Leucocytozoon) can regulate passerine populations. Thus, reduction in the number of avian haemosporidian infections in a population, for example in recently introduced hosts, may facilitate host establishment or spread (i.e. enemy release). Alternatively, colonizers could decrease competitive ability of native individuals in the novel range by increasing the prevalence of avian haemosporidians in that native passerine community (i.e. novel weapons). However, whether either or both of these phenomena will occur is difficult to predict because infection risk can be highly heterogeneous and dependent upon the interaction of biotic and abiotic factors at the microclimate level, especially because of the important role of vectors for these parasites. Here, we describe which factors best predicted avian haemosporidian prevalence in populations of house sparrows Passer domesticus introduced to Kenya. House sparrows inhabit an invasion gradient in Kenya; they were introduced via the eastern port city of Mombasa in ? 1950 and have since spread west‐ward across the country. This range expansion gave us the opportunity to examine how parasite prevalence changes over small spatiotemporal scales and what role is played by environmental and individual traits. Among all individuals, body mass was the strongest predictor of infection, with larger house sparrows being more likely to be infected. At the population level, capture month, precipitation (higher prevalence with more rainfall), and population age (increasing prevalence with increasing time since introduction) were important risk factors. Overall, haemosporidian prevalence in Kenyan house sparrows appears to be more strongly associated with individual characteristics rather than with time since introduction as was predicted, though this does not necessarily rule out a role for enemy release or novel weapons in this system.     

Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus

Little is known about the development of infection of malaria parasites of the genus Plasmodium in wild birds. We used qPCR, targeting specific mitochondrial lineages of Plasmodium ashfordi (GRW2) and Plasmodium relictum (GRW4), to monitor changes in intensities of parasitemia in captive great reed warblers Acrocephalus arundinaceus from summer to spring. The study involved both naturally infected adults and experimentally infected juveniles. The experiment demonstrated that P. ashfordi and P. relictum lineages differ substantially in several life-history traits (e.g. prepatent period and dynamics of parasitemia) and that individual hosts show substantial differences in responses to these infections. The intensity of parasitemia of lineages in mixed infections co-varied positively, suggesting a control mechanism by the host that is general across the parasite lineages. The intensity of parasitemia for individual hosts was highly repeatable suggesting variation between the host individuals in their genetic or acquired control of the infections. In future studies, care must be taken to avoid mixed infections in wild caught donors, and when possible use mosquitoes for the experiments as inoculation of infectious blood ignores important initial stages of the contact between the bird and the parasite.     

Are chronic avian haemosporidian infections costly in wild birds?

One group of commonly found parasites in birds, for which fitness consequences and effects on life history traits have been much debated are Haemosporidian blood parasites. In a long term study population of great reed warblers Acrocephalus arundinaceus in Sweden, previous studies have shown that the Haemosporidian blood parasites are in their chronic phase during the breeding season and that the fitness of infected and non‐infected birds are similar. In the present study, we quantified parasite intensity (parasitemia) in 718 adults great reed warblers sampled between 1987 and 1998 for the three most common parasite species; Haemoproteus payevskyi (lineage GRW1), Plasmodium ashfordi (GRW2) and Plasmodium relictum (GRW4). We verified that the q‐PCR method is accurately quantifying Haemoproteus payevskyi (GRW1) as it was highly correlated with the number of parasites seen under microscope. Frequency of mixed infections with two lineages was significantly higher than expected based on the prevalence of each of the three parasite lineages. The mean level of parasitemia was significantly different for the three lineages and individual birds had repeatable parasitemia levels between years. Females tended to have a higher parasitemia than males for all three parasite lineages combined. Females with higher GRW1 parasitemia tended to arrive later in spring to their breeding sites. There was a negative correlation between parasitemia and number of fledged offspring for GRW1, and a tendency for a negative correlation between GRW2 parasitemia and the proportion of recruiting offspring. Overall our results demonstrate that chronic Haemosporidian infections can have slight but significant effects on host life history traits, and therefore may act as important selective agents in wild bird populations.     

Patterns of hatching failure in the house sparrow Passer domesticus

Hatching failure is widespread in birds despite presumably strong selection against any wasted reproductive effort and yet there have been few attempts at uncovering sources of variation in failure within a species. Here we use 11 yr of data on the frequency of both undeveloped and unhatched eggs in a marked population of house sparrows Passer domesticus to examine the effects of multiple factors hypothesized to affect hatching success in birds including parental identity, phenotype and genotype, as well as several environmental variables. Unhatched eggs were present in 34.3% of 1523 clutches in which at least one egg hatched, and a total of 10.1% of eggs failed to hatch, of which 75.7% had no visible embryo. We found an effect of female identity on the proportion of eggs that developed and an effect of male identity on hatching success, as well as a positive effect of egg size on both the proportion of eggs that developed and hatching success between females. Neither the proportion of eggs that developed nor hatching success varied according to time of season or weather conditions, clutch size, the age of either parent, the size of the male's black bib, female size, female heterozygosity or the genetic similarity between members of a pair. There was also no positional bias in the occurrence of undeveloped eggs, although undeveloped eggs were more common among birds nesting at low density. Our results suggest that hatching failure in house sparrows has few environmental components and is primarily influenced by intrinsic differences among individuals.     

Diversity, loss, and gain of malaria parasites in a globally invasive bird

Invasive species can displace natives, and thus identifying the traits that make aliens successful is crucial for predicting and preventing biodiversity loss. Pathogens may play an important role in the invasive process, facilitating colonization of their hosts in new continents and islands. According to the Novel Weapon Hypothesis, colonizers may out-compete local native species by bringing with them novel pathogens to which native species are not adapted. In contrast, the Enemy Release Hypothesis suggests that flourishing colonizers are successful because they have left their pathogens behind. To assess the role of avian malaria and related haemosporidian parasites in the global spread of a common invasive bird, we examined the prevalence and genetic diversity of haemosporidian parasites (order Haemosporida, genera Plasmodium and Haemoproteus) infecting house sparrows (Passer domesticus). We sampled house sparrows (N = 1820) from 58 locations on 6 continents. All the samples were tested using PCR-based methods; blood films from the PCR-positive birds were examined microscopically to identify parasite species. The results show that haemosporidian parasites in the house sparrows'' native range are replaced by species from local host-generalist parasite fauna in the alien environments of North and South America. Furthermore, sparrows in colonized regions displayed a lower diversity and prevalence of parasite infections. Because the house sparrow lost its native parasites when colonizing the American continents, the release from these natural enemies may have facilitated its invasion in the last two centuries. Our findings therefore reject the Novel Weapon Hypothesis and are concordant with the Enemy Release Hypothesis.