Leonard A. Freed

Evolutionary ecology and radiation of Hawaiian passerine birds.

The Hawaiian islands contain the most spectacular variety of landbirds ever discovered on remote oceanic islands. The Hawaiian honeycreepers, having evolved from a presumably single founding species of cardueline finch, comprise most of this avifauna. Birds from at least three other families of passerines and five families of non-passerines also radiated in Hawaii. Recent discoveries of a fossil avifauna indicate that most radiations were more extensive than previously thought. Classical analysis of the radiation of Hawaiian birds, especially the honeycreepers, focused on characters related to acquisition of food. Recent studies of bill size and shape in relation to food resources, and of foraging mode in relation to interspecific competitors, provide models of how divergence in diet and/or bill morphology might have evolved. Studies of geographic variation among subspecies on different islands and among populations within islands have revealed extensive divergence in characters such as sexual chromatism, nest sites and nest morphology.

INCREASE IN AVIAN MALARIA AT UPPER ELEVATION IN HAWAI'I

Abstract Hawaiian honeycreepers (Aves: Drepanidinae) evolved in the absence of mosquito-borne diseases such as avian malaria (Plasmodium spp.). Malaria has been largely responsible for the recent wave of extinctions and endangerment among Hawaiian forest birds, which began by the 1920s. Most honeycreepers, especially endangered species, now persist only in forests above 1500 m elevation, where cool temperatures prevent effective malaria development in mosquitoes. We report here that prevalence of malaria in Hawaiian forest birds at 1900 m on the island of Hawai‘i has more than doubled over a decade. This increase was associated with breeding of mosquitoes and warmer summertime air temperatures. We also report direct evidence of tolerance to malaria, and a possible cost of tolerance, in wild native birds. Tolerance is adding to a reservoir of malaria at upper elevations even while vectors are rare and air temperatures are too low for complete development of the parasite in the vector. The data provide a glimpse of how malaria is becoming an emergent infectious disease at upper elevations.

THE LONG-TERM PAIR BOND OF TROPICAL HOUSE WRENS: ADVANTAGE OR CONSTRAINT?

Permanent monogamy may be the most prevalent mating system in birds because most birds are tropical residents found as pairs in territories that are defended throughout the year. Long-term pair bonds may be advantageous to individuals with respect to current and future reproductive success. Conversely, each member may be constrained to remain with the current mate because of limited opportunities to acquire new mates. These alternative hypotheses were evaluated for permanently monogamous tropical house wrens in lowland central Panama. Mates gain no reproductive advantage by reuniting from one breeding season to the next or by reuniting within breeding seasons. In contrast, the scarcity of openings within the stable breeding population limits the opportunities for each sex to re-sort. Moreover, pairs must guard against encroachment by neighboring pairs and takeover by non-neighboring pairs. The same constraints that shape the long-term pair bond appear to influence the structure of the floater population, which includes transient pairs as well as individuals. Mates usually do not defend each other against single intruders, even when takeovers occur, suggesting that mate choice is a recurring phenomenon even in this permanently monogamous mating system. These results probably pertain to other tropical monogamous species with long-term pair bonds, but detailed studies of other species are required to establish generality.

DNA QUALITY AND ACCURACY OF AVIAN MALARIA PCR DIAGNOSTICS: A REVIEW

Abstract Birds have become increasingly prominent in studies focusing on natural populations and their coevolved pathogens or examining populations under environmental stress from novel and emerging infectious diseases. For either type of study, new DNA-based diagnostic tests, using the polymerase chain reaction (PCR), present challenges in detecting the DNA of pathogens, which exist in low copy number compared with DNA of the host. One example comes from studies of avian malaria: conflicting claims are made by different laboratories about the accuracy of tests using various sets of primers and reagents, especially in relation to blood smears and immunological methods. There is little standardization of protocol or performance among laboratories conducting tests, in contrast to studies of human malaria. This review compares the problems of detecting avian malaria with those of detecting human malaria, and shows definitively that the buffer used to store blood samples following collection is associated with the accuracy of the test. Lower accuracy is associated with use of a lysis buffer, which apparently degrades the DNA in the blood sample and contributes to inhibition of PCR reactions. DNA extraction and purification techniques, and optimization of the PCR reaction, do not appear to be alternative explanations for the effect of storage buffer. Nevertheless, the purest DNA in standard concentrations for PCR is required so that different primers, DNA polymerases, and diagnostic tests can be objectively compared.

Negative Effects of an Introduced Bird Species on Growth and Survival in a Native Bird Community

Exploitative competition is a major determinant of community structure in natural assemblages [1, 2], but, introduced species are rarely competitors that lead to extinction of native species [3, 4]. Here we document strong community-wide competition from the Japanese white-eye (Zosterops japonicus) on native Hawaiian passerine birds. Introduced in 1929 [5], white-eye successfully invaded old-growth forest and coexisted with eight native species [6], overlapping multiple foraging substrates with each but evidencing no agonistic interactions [7]. The endangered Hawaii akepa (Loxops coccineus coccineus) was viable during 1987-1999 but became nonviable during 2000-2006 in association with an abrupt increase in white-eyes [7]. We show that after 2000, juveniles of every native bird species measured had lower mass and shorter bills and tarsi. For most species, lower mass led to decreased juvenile survival, and shorter bills to decreased survival of second-year and older adults. Lower survival of smaller birds represents normalizing selection that is restoring previous size means to future generations [8]. Birds at a nearby site with fewer white-eyes had normal size. White-eye had less stunting of bills and did not suffer the survival consequences of native species. Exploitative competition for food between native birds and an introduced species requires intensive management to prevent further declines.

STRUCTURE AND DYNAMICS OF MIXED-SPECIES FLOCKS IN A HAWAIIAN RAIN FOREST

Abstract Mixed-species flocks of native and introduced birds were studied for four years in an upper elevation Hawaiian rain forest. Those flocks were characterized by strong seasonality, large size, low species richness, high intraspecific abundance, a lack of migrants, and a general lack of territoriality or any sort of dominance hierarchy. There was high variability among years in patterns of occurrence at the species level, and high variability within years at the individual level. These flocks are loosely structured social groupings with apparently open membership. The fluid, unstable movement patterns, high degree of variability in size and composition, and lack of positive interspecific associations are not consistent with the “foraging enhancement” hypothesis for flocking. Two resident, endangered insectivores, the Akepa (Loxops coccineus) and Hawaii Creeper (Oreomystis mana) served as “nuclear” species. Flock composition was compared between two study sites that differed significantly in density of these two nuclear species. Flock size was similar at the two sites, primarily because the nuclear species were over-represented relative to their density. This observation suggests that birds are attempting to achieve a more optimal flock size at the lower density site.

Variation in male plumage and behavior of the Hawaii Akepa

-The sexually dichromatic and endangered Island of Hawaii subspecies of Akepa (Loxops coccineus coccineus) is a 10to 12-g Hawaiian honeycreeper that shows remarkable variation in male plumage coloration, ranging from dull gray to bright orange. We found that this variation is primarily due to a two-year delay in plumage maturation by young males. Second-year males possess a mainly grayish-green plumage that is similar to that of females, and rarely try to breed. Third-year males have a partially orange plumage that is intermediate between that of females and adult males, and competently breed in small numbers. In addition, there are variations within age classes that reflect alternative life histories and perhaps diet. The existence of both femalelike and malelike subadult plumage in a population is unlike North American passerines with delayed plumage maturation, especially cardueline finches, which are considered to be the closest relatives of the Hawaiian honeycreepers. The extreme delay is associated with high survivorship, strong philopatry, and a varied prebreeding competition among males that includes group displays and which lasts for six months or more each year. These characteristics are common in lekking or cooperatively breeding species, but are unusual for a small, monogamous passerine with biparental care. Received 1 October 1993, accepted 11 January 1994. FEW PHENOTYPIC CHARACTERS SO closely track the life history and social system of birds as do color and brightness of plumage (Baker and Parker 1979, Rohwer and Butcher 1988, Butcher and Rohwer 1989). Plumage can make an individual more or less conspicuous to predators, ecological competitors, sexual rivals, and potential mates, and may reflect a genotype that has superior tolerance of or resistance to diseases and parasites (Hamilton and Zuk 1982). The relation between plumage and reproductive maturity also has been identified as an example of paedomorphosis or heterochrony in birds (Lawton and Lawton 1986). Whereas birds typically reach adult size within a year after fledging, individuals may become sexually mature before acquiring terminal adult plumage. Delayed maturation of plumage, appropriately identified as a neotenic character, has been documented in numerous avian orders and families and has been shown to be related to complexity of social organization (Lawton and Lawton 1986) and to intensity of sexual selection (Selander 1965, Rohwer et al. 1980, Studd and Robertson

Prospective Infanticide and Protection of Genetic Paternity in Tropical House Wrens

Sexually selected infanticide occurs when adults kill dependent offspring of potential mates and initiate new reproductive attempts with those mates more rapidly than if they had waited for the offspring tobecome independent (Hrdy 1974, 1979). In this context, infanticide usually occurs when immatures or eggs are visible at the time the killing adult replaces the preceding breeder. Prospective infanticide can be defined as a subset of sexually selected infanticide in which young born or eggs laid after mate replacement are killed. For such infanticide to be adaptive, males must somehow evaluate paternity by killing only offspring that appear within one gestation period (mammals) or one fertility period (birds). Although a wide variety of mammals (Hrdy 1979; Sherman 1981; papers in Hausfater and Hrdy 1984) and birds (Crook and Shields 1985; Freed 1986a; reviewed in Rohwer 1985) are known to kill young visible at the time of replacement, prospective infanticide is known only in two species of mammals (lions [Panthera leo], Bertram 1975; Packer and Pusey 1983; and Hanuman langurs [Presbytis entellus], Sommer and Mohnot 1985; but cf. Hrdy 1979). Nevertheless, prospective infanticide is assumed to occur more widely and to influence female reproductive strategies in populations in which sexually selected infanticide has evolved (Hrdy 1977, 1979; Labov 1981; Hausfater 1984). In this paper I document prospective infanticide of eggs laid several days after the appearance of new males in tropical house wrens (Troglodytes aedon). The avian cases extend the generality of the phenomenon and show that males have the ability to evaluate paternity by behaving differently toward eggs appearing within and just after one short fertile period following replacement.

Explosive Increase in Ectoparasites in Hawaiian Forest Birds

Ectoparasites, particularly chewing lice in the Phthiraptera (Insecta), affect the ecology of numerous host species. Most lice are highly host-specific, and there are no documented cases of major increases of chewing lice, within populations, over years. During continuous study from 1987–2005 at upper elevation forests on the island of Hawaii, chewing lice were exceedingly rare and, until 2003, were found in just 2 of 12 species of native and introduced birds. From 2003–2005, there was an explosive increase in the prevalence of chewing lice in all host species. There was no change in humidity, or in behavior of hosts, that could have caused an ecological release of existing lice. Based on reduced fat levels and increases in broken wing and tail feathers for most host species, there was apparently a food limitation that preceded the increase. The increase coincided temporally with detection of a nonnative bird that had recently been found in elevations below the study sites. Although there were isolated sightings of this bird on the study sites, seasonal movements and behavior of some species of native birds could also have allowed greater transmission to study sites. Both prevalence and intensity of infection, indexed by number of body regions parasitized, were lower in native species with greater bill overlap, a character that could help birds control lice. Seasonality of prevalence indicated that low prevalence preceded molt and high prevalence occurred after molting of hosts. The number of major fault bars in wing and tail feathers, a sign of nutritive stress, was correlated with intensity of infection, indicating an indirect cost to the hosts of being parasitized. In addition, birds with lice were less likely to be recaptured than birds without lice.

Changes in Timing, Duration, and Symmetry of Molt of Hawaiian Forest Birds

Food limitation greatly affects bird breeding performance, but the effect of nutritive stress on molt has barely been investigated outside of laboratory settings. Here we show changes in molting patterns for an entire native Hawaiian bird community at 1650–1900 m elevation on the Island of Hawaii between 1989–1999 and 2000–2006, associated with severe food limitation throughout the year beginning in 2000. Young birds and adults of all species took longer to complete their molt, including months never or rarely used during the 1989–1999 decade. These included the cold winter months and even the early months of the following breeding season. In addition, more adults of most species initiated their molt one to two months earlier, during the breeding season. Suspended molt, indicated by birds temporarily not molting primary flight feathers during the months of peak primary molt, increased in prevalence. Food limitation reached the point where individuals of all species had asymmetric molt, with different primary flight feathers molted on each wing. These multiple changes in molt, unprecedented in birds, had survival consequences. Adult birds captured during January to March, 2000–2004, had lower survival in four of five species with little effect of extended molt. Extended molt may be adaptive for a nutrient stressed bird to survive warm temperatures but not cool winter temperatures that may obliterate the energy savings. The changing molt of Hawaiian birds has many implications for conservation and for understanding life history aspects of molt of tropical birds.