Endangered and Threatened Wildlife and Plants; Threatened Species Status for the Iiwi (Drepanis coccinea), 43873-43885 [2017-20074]

Agencies

• Fish and Wildlife Service
• DEPARTMENT OF THE INTERIOR

[Federal Register Volume 82, Number 181 (Wednesday, September 20, 2017)]
[Rules and Regulations]
[Pages 43873-43885]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2017-20074]



[[Page 43873]]

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DEPARTMENT OF THE INTERIOR

Fish and Wildlife Service

50 CFR Part 17

[Docket No. FWS-R1-ES-2016-0057; 4500030113]
RIN 1018-BB54


Endangered and Threatened Wildlife and Plants; Threatened Species 
Status for the Iiwi (Drepanis coccinea)

AGENCY: Fish and Wildlife Service, Interior.

ACTION: Final rule.

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SUMMARY: We, the U.S. Fish and Wildlife Service (Service), determine 
threatened status under the Endangered Species Act of 1973, as amended 
(Act), for the iiwi (Drepanis coccinea), a bird species from the 
Hawaiian Islands. The effect of this regulation is to add this species 
to the Federal List of Endangered and Threatened Wildlife.

DATES: This rule becomes effective October 20, 2017.

ADDRESSES: This final rule is available on the internet at https://www.regulations.gov and https://www.fws.gov/pacificislands. Comments and 
materials we received, as well as supporting documentation we used in 
preparing this rule, such as the species status report, are available 
for public inspection at https://www.regulations.gov. Comments, 
materials, and documentation that we considered in this rulemaking will 
be available by appointment, during normal business hours at: U.S. Fish 
and Wildlife Service, Pacific Islands Fish and Wildlife Office, 300 Ala 
Moana Boulevard, Room 3-122, Honolulu, HI 96850; by telephone at 808-
792-9400; or by facsimile at 808-792-9581.

FOR FURTHER INFORMATION CONTACT: Mary Abrams, Field Supervisor, Pacific 
Islands Fish and Wildlife Office, 300 Ala Moana Boulevard, Room 3-122, 
Honolulu, HI 96850; by telephone (808-792-9400); or by facsimile (808-
792-9581). Persons who use a telecommunications device for the deaf 
(TDD) may call the Federal Relay Service (FIRS) at 800-877-8339.

SUPPLEMENTARY INFORMATION: 

Executive Summary

    Why we need to publish a rule. Under the Endangered Species Act, 16 
U.S.C. 1531 et seq., a species or subspecies may warrant protection 
through listing if it is endangered or threatened throughout all or a 
significant portion of its range. Critical habitat shall be designated, 
to the maximum extent prudent and determinable, for any species 
determined to be an endangered or threatened species under the Act.
    This rule finalizes the listing of the iiwi (Drepanis coccinea) as 
threatened under the Act because of current and future threats, and 
listing can only be done by issuing a rule. The iiwi no longer occurs 
across much of its historical range, and faces a variety of threats in 
the form of diseases and impacts to its remaining habitat.
    Delineation of critical habitat requires, within the geographical 
area occupied by the species, identification of the physical or 
biological features essential to the species' conservation. A careful 
assessment of the biological needs of the species and the areas that 
may have the physical or biological features essential for the 
conservation of the species and that may require special management 
considerations or protections, and thus qualify for designation as 
critical habitat, is particularly complicated in this case by the 
ongoing and projected effects of climate change and will require a 
thorough assessment. We require additional time to analyze the best 
available scientific data in order to identify specific areas 
appropriate for critical habitat designation and to analyze the impacts 
of designating such areas as critical habitat. Accordingly, we find 
designation of critical habitat for the iiwi to be ``not determinable'' 
at this time.
    What this document does. This document lists the iiwi as a 
threatened species. We previously published a 90-day finding and a 12-
month finding and proposed listing rule for the iiwi. Those documents 
assessed all available information regarding status of and threats to 
the iiwi.
    The basis for our action. Under the Act, we can determine that a 
species is an endangered or threatened species based on any of five 
factors: (A) The present or threatened destruction, modification, or 
curtailment of its habitat or range; (B) Overutilization for 
commercial, recreational, scientific, or educational purposes; (C) 
Disease or predation; (D) The inadequacy of existing regulatory 
mechanisms; or (E) Other natural or manmade factors affecting its 
continued existence. We have determined that the primary threats to the 
iiwi are its susceptibility to avian malaria (Factor C) and the 
expected reduction in disease-free habitat as a result of increased 
temperatures caused by climate change (Factor E). Although not 
identified as primary threat factors, rapid ohia death, a fungal 
disease that kills the tree species required by iiwi for nesting and 
foraging, and impacts from nonnative invasive plants and feral 
ungulates, contribute to the degradation and curtailment of the iiwi's 
remaining, disease-free native ohia forest habitat, exacerbating 
threats to the species' viability.
    Peer review and public comment. We sought comments on our proposal 
from eight independent specialists to ensure that our designation is 
based on scientifically sound data, assumptions, and analyses. We also 
considered all comments and information received during the public 
comment period.
    A species status report for the iiwi was prepared by a team of 
Service biologists, with the assistance of scientists from the U.S. 
Geological Survey's (USGS) Pacific Islands Ecosystems Research Center 
and the Service's Pacific Islands Climate Change Cooperative. We also 
obtained review and input from experts familiar with avian malaria and 
avian genetics. The species status report represents a compilation of 
the best scientific and commercial data available concerning the status 
of the species, including the past, present, and future threats to the 
iiwi. The final species status report, revised in response to peer 
reviewer comments, and other materials relating to this proposal can be 
found at https://www.regulations.gov, at Docket No. FWS-R1-ES-2016-0057, 
or by contacting the Pacific Islands Fish and Wildlife Office (see FOR 
FURTHER INFORMATION CONTACT).

Background

Previous Federal Actions

    Please refer to the proposed listing rule, published in the Federal 
Register on September 20, 2016 (81 FR 64414), for previous Federal 
actions for this species prior to that date. The publication of the 
proposed listing rule opened a 60-day public comment period that closed 
on November 21, 2016. We published a public notice of the proposed rule 
on September 19, 2016. This notice was picked up and published by 
several local media outlets including the State's largest newspaper, 
the Honolulu Star Advertiser, as well as the Garden Island Newspaper, 
Honolulu Civil Beat, and Hawaii News Now.

Summary of Comments and Recommendations

    We solicited comments during the 60-day public comment period from 
September 20, to November 21, 2016 (81 FR 64414). We contacted 
appropriate Federal and State agencies, scientific experts and 
organizations, and other interested parties and invited them to

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comment on the proposal. Notices inviting public comment also were 
published in four major news outlets in the State. During the comment 
period, we received a total of nine letters from members of the public. 
We did not receive any requests for a public hearing. In this final 
rule, we address only those comments directly relevant to the listing 
of the iiwi. All nine letters were from individual members of the 
public. We did not receive any comments from the State of Hawaii.

Public Comments

    Of the nine comment letters we received from members of the public, 
eight expressed general support for our listing the iiwi under the Act, 
and one commented on a topic unrelated to our proposed rule. None of 
these letters provided new, substantive information or comments 
requiring specific response here.

Peer Review

    In accordance with our peer review policy published on July 1, 1994 
(59 FR 34270), we solicited expert opinions from eight individuals with 
scientific expertise on the iiwi and its habitat, biological needs, and 
threats, including familiarity with the geographic region where the 
iiwi occurs, and principles of conservation biology. We received 
responses from all eight of these individuals.
    In general, all of the peer reviewers agreed that the draft Species 
Status Report and proposed rule provided an accurate synthesis of the 
life history of the iiwi and robust analysis of the stressors affecting 
the species. They further agreed that our conclusions regarding the 
status of the species were reasonable and scientifically sound. We 
reviewed all comments received from the peer reviewers for substantive 
issues and new information regarding the listing of iiwi. Where 
appropriate, we have incorporated corrections, editorial suggestions, 
and new literature and other information they provided into both the 
final species report and final rule. Any substantive comments are 
discussed below (see also Summary of Changes from Proposed Rule). All 
of the peer reviews were constructive and thorough; we thank the peer 
reviewers for their thoughtful assistance.
    Comment (1): Two of the peer reviews suggested that we had not 
sufficiently emphasized the potential importance of avian pox as a 
threat to the iiwi. Specifically, the reviewers noted that the 
literature on mosquito-borne diseases affecting native Hawaiian forest 
birds tends to be focused more on avian malaria due, in part, to the 
knowledge gaps about the impacts of avian pox and the lack of an 
accurate, noninvasive diagnostic test for identifying acute active 
infections and birds that have recovered from infection. The reviewers 
point out that the two diseases may be acting both individually and 
synergistically when infections are simultaneous. Although avian 
malaria has been more thoroughly studied, the peer reviewers felt that 
the available evidence suggests avian pox may also be a significant 
source of mortality and pose a greater threat to the iiwi than would be 
suggested by our analysis.
    Our Response: Although our draft Species Status Report pointed to 
the difficulty in untangling the relationship between the two diseases 
because of their frequent occurrence together, we agree with the 
reviewers that we placed more emphasis on the threat posed by avian 
malaria, in part simply due to the greater amount of scientific 
information available that clearly links high levels of mortality in 
iiwi directly to infection with malaria. In our final Species Status 
Report and this final rule, we have increased emphasis on the 
possibility that avian pox, both alone and in combination with avian 
malaria, may have negative, population-level impacts on iiwi.
    Comment (2): One reviewer suggested that the ``estimate'' of 50 
birds on Oahu reported in the draft Species Status Report is 
unrealistically high and not based on scientific data; the reviewer 
stated that based on observations of occasional single birds over the 
past 15 years, the population is probably much less than 50, perhaps 10 
at the most. Likewise for Molokai, the reviewer pointed out that the 
estimated number of birds from the 1980s is no longer accurate, and 
there are many fewer than 80 birds on that island.
    Our Response: We thank the reviewer for his comments, and have made 
the corrections as needed in the final Species Status Report. Because 
the proposed rule did not refer to specific numbers of birds, no 
associated changes were required in this final rule.
    Comment (3): Two peer reviewers provided updated information 
regarding the impacts and extent of various diseases affecting ohia 
trees, especially rapid ohia death (also known as ohia wilt, caused by 
fungi in the genus Ceratocystis).
    Our Response: We have incorporated these changes into the final 
Species Status Report and final rule, as appropriate. In particular, we 
have updated the estimated area infected with rapid ohia death on 
Hawaii Island to more than 50,000 acres (20,235 hectares) (Hughes 2016, 
pers. comm.).
    Comment (4): One peer reviewer pointed out that, although Paxton et 
al. (2013) stated that the iiwi population on the leeward (Kona) side 
of Hawaii Island is strongly increasing, they couched those specific 
results as the inference from a limited dataset. The reviewer suggested 
that it was important for us to provide a similar caveat with regard to 
this reported trend in our final Species Status Report and final rule.
    Our Response: We agree that this point provides important context 
for the interpretation of this reported trend, and have provided 
additional language in the final Species Status Report and in this 
final rule to more accurately mirror the reported results of Paxton et 
al. 2013.
    Comment (5): One peer reviewer suggested that, although it is true 
that the effects of predation have not been well documented or 
quantified for the iiwi, there is substantial evidence that predation 
by nonnative rats, particularly the black rat (Rattus rattus), is a 
serious threat to other Hawaiian forest birds. Although the reviewer 
acknowledges that predation is difficult to detect and document, 
particularly in species like the iiwi that nest high in the forest 
canopy, he believes the available evidence suggests predation by rats 
is likely also a contributing factor in the decline of the iiwi.
    Our Response: We have incorporated additional discussion of the 
potential impacts of rat predation on the iiwi in this final rule.
    Comment (6): Two peer reviewers suggested that we consider the 
findings of Paxton et al. (2016) in a paper published subsequent to the 
writing of our draft Species Status Report.
    Our Response: We have incorporated the results of Paxton et al. 
2016 into our final Species Status Report and this final rule. This 
research documents the rapid collapse of the native avian community on 
the island of Kauai since 2000 as a result of the impacts of mosquito-
borne diseases exacerbated by increased ambient temperature. In 
particular, the projections of Paxton et al. (2016) point to the likely 
extirpation of the iiwi from the island of Kauai by the year 2050 as a 
consequence of the loss of disease-free habitat on Kauai and consequent 
exposure to avian malaria and pox. We also updated the reported numbers 
and range of iiwi on Kauai with the more recent estimates from Paxton 
et al. (2016).

Summary of Changes From Proposed Rule

    After consideration of the comments we received during the public 
comment period and new information published

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or obtained since the proposed rule was published, we have made some 
changes to the final rule. None of these changes affect the 
determination. We made many small, nonsubstantive changes and 
corrections (e.g., updating the Background section in response to 
comments, minor clarifications, and editorial changes) throughout the 
document. In addition, we made some substantive changes to the 
information in this final rule in response to peer review, which are 
summarized here:
    (1) We have elevated the identification of avian pox as a 
potentially important factor contributing to the decline of iiwi in 
response to mosquito-borne diseases, in addition to the effects of 
avian malaria;
    (2) We have made a more definitive statement about the likely 
negative effects of rat predation on iiwi (VanderWerf 2016, pers. 
comm.);
    (3) We updated the amount of area on Hawaii Island that is now 
estimated to be affected by rapid ohia death, which has now increased 
to more than 50,000 acres (20,235 hectares) (Hughes 2016, pers. comm.);
    (4) We have updated our discussion of both the documented and 
projected declines of native forest birds on the island of Kauai to 
reflect the recently published work of Paxton et al. (2016), which 
projects the potential extirpation of iiwi from that island by the year 
2050 as a consequence of warming temperatures and associated exposure 
to mosquito-borne diseases.

Status Assessment for the Iiwi

    A thorough review of the taxonomy, life history, and ecology of the 
iiwi (Drepanis coccinea) is presented in the Iiwi (Drepanis coccinea) 
Species Status Report, available online at https://www.regulations.gov 
under Docket No. FWS-R1-ES-2016-0057. The species status report 
documents the results of our comprehensive biological status review for 
the iiwi, including an assessment of the potential stressors to the 
species. The species status report does not represent a decision by the 
Service on whether the iiwi should be listed as a threatened or 
endangered species under the Act; that decision involves the 
application of standards within the Act and its implementing 
regulations and policies. The species report does, however, provide the 
scientific basis that informs our regulatory decision. We have revised 
the report in response to comments from peer reviewers, who provided 
new information, additional references, and minor corrections. None of 
these changes substantively altered the conclusions we drew from the 
available information or changed the outcome of our assessment. The 
following is a summary of the key results and conclusions from the 
species status report.

Summary of Biological Status

    A medium-sized forest bird notable for its iconic bright red 
feathers, black wings and tail, and a long, curved bill (Fancy and 
Ralph 1998, p. 2), the iiwi belongs to the family Fringillidae and the 
endemic Hawaiian honeycreeper subfamily, Drepanidinae (Pratt et al. 
2009, pp. 114, 122). Iiwi songs are complex with variable creaks (often 
described as sounding like a ``rusty hinge''), whistles, or gurgling 
sounds, and they sometimes mimic other birds (Fancy and Ralph 1998, p. 
5; Hawaii Audubon Society 2011, p. 97). The species is found primarily 
in closed canopy, montane wet or montane mesic forests composed of tall 
stature ohia (Metrosideros polymorpha) trees or ohia and koa (Acacia 
koa) tree mixed forest. The iiwi's diet consists primarily of nectar 
from the flowers of ohia and mamane (Sophora chrysophylla), various 
plants in the lobelia (Campanulaceae) family (Pratt et al. 2009, p. 
193), and occasionally, insects and spiders (Fancy and Ralph 1998, pp. 
4-5; Pratt et al. 2009, p. 193).
    Although iiwi may breed anytime between October and August (Fancy 
and Ralph 1998, p. 7-8), the main breeding season occurs between 
February and June, which coincides with peak flowering of ohia (Fancy 
and Ralph 1997, p. 2). Iiwi create cup-shaped nests typically within 
the upper canopy of ohia (Fancy and Ralph 1998, p. 7-8), and breeding 
pairs defend a small area around the nest and disperse after the 
breeding season (Fancy and Ralph 1997, p. 2). An iiwi clutch typically 
consists of two eggs, with a breeding pair raising one to two broods 
per year (Fancy and Ralph 1998, p. 7-8).
    Well known for their seasonal movements in response to the 
availability of flowering ohia and mamane, iiwi are strong fliers that 
move long distances following their breeding season to locate nectar 
sources (Fancy and Ralph 1998, p. 3; Kuntz 2008, p. 1; Guillamet et al. 
2016, p. 192). The iiwi's seasonal movement to lower elevation areas in 
search of nectar sources is an important factor in the exposure of the 
species to avian diseases, particularly malaria (discussed below).
    Although historical abundance estimates are not available, the iiwi 
was considered one of the most common of the native forest birds in 
Hawaii by early naturalists, described as ``ubiquitous'' and found from 
sea level to the tree line across all the major islands (Banko 1981, 
pp. 1-2). Today the iiwi is no longer found on Lanai, and only a few 
individuals may be found on Oahu, Molokai, and west Maui. Remaining 
populations of iiwi are largely restricted to forests above 
approximately 3,937 feet (ft) (1,200 meters (m)) in elevation on Hawaii 
Island (Big Island), east Maui, and Kauai. As described below, the 
present distribution of iiwi corresponds with areas that are above the 
elevation at which the transmission of avian malaria readily occurs 
(``disease-free'' habitats). The current abundance of iiwi rangewide is 
estimated at a mean of 605,418 individuals (range 550,972 to 659,864). 
Ninety percent of all iiwi now occur on Hawaii Island, followed by east 
Maui (about 10 percent), and Kauai (less than 1 percent) (Paxton et al. 
2013, p. 10; Paxton et al. 2016, p. 2).
    Iiwi population trends and abundance vary across the islands. The 
population on Kauai appears to be in steep decline, with a modeled rate 
of decrease equivalent to a 92 percent reduction in population over a 
25-year period (Paxton et al. 2013, p. 10); the total population on 
Kauai is estimated at a mean of 2,603 birds (range 1,789 to 3,520) 
(Paxton et al. 2016, p. 2). Trends on Maui are mixed, but populations 
there generally appear to be in decline; East Maui supports an 
estimated population of 59,859 individuals (range 54,569 to 65,148) 
(Paxton et al. 2013, p. 10). On Hawaii Island, which supports the 
largest remaining numbers of iiwi at an estimated average of 543,009 
individuals (range 516,312 to 569,706), evidence exists for stable or 
declining populations on the windward side of the island. Strong trends 
of increase are inferred on the leeward (Kona) side of the island, but 
these trends should be interpreted with caution because they are based 
on a limited number of surveys (Paxton et al. 2013, pp. 25-26; Camp 
2016, pers. comm.). As noted above, iiwi have been extirpated from 
Lanai, and only a few individual birds have been sporadically detected 
on the islands of Oahu, Molokai, and on west Maui in recent decades. Of 
the nine iiwi population regions for which sufficient information is 
available for quantitative inference, five of those show strong or very 
strong evidence of declining populations; one, a stable to declining 
population; one, a stable to increasing population; and two, strong 
evidence for increasing populations. Four of the nine regions show 
evidence of range contraction. Overall, based on the most recent 
surveys (up to 2012), approximately 90 percent of remaining

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iiwi are restricted to forest within a narrow band between 4,265 and 
6,234 ft (1,300 and 1,900 m) in elevation (Paxton et al. 2013, pp. 1, 
10-11, and Figure 1) (See the Population Status section of the species 
status report for details).

Summary of Factors Affecting the Species

    The Act directs us to determine whether any species is an 
endangered species or a threatened species because of any of five 
various factors affecting its continued existence. Our species status 
report evaluated many potential stressors to iiwi, particularly direct 
impacts on the species from introduced diseases, as well as predation 
by introduced mammals, competition with nonnative birds, climate 
change, ectoparasites, and the effects of small population size. We 
also assessed stressors that may affect the extent or quality of the 
iiwi's required ohia forest habitat, including ohia dieback (a natural 
phenomenon), ohia rust (a nonnative pathogen), drought, fires, volcanic 
eruptions, climate change, and particularly rapid ohia death (ROD, also 
known as ohia wilt; a nonnative pathogen) and habitat alteration by 
nonnative plants and feral ungulates.
    All species experience stressors; we consider a stressor to rise to 
the level of a threat to the species if the magnitude of the stressor 
is such that it places the current or future viability of the species 
at risk. In considering what stressors or factors might constitute 
threats to a species, we must look beyond the exposure of the species 
to a particular stressor to evaluate whether the species may respond to 
that stressor in a way that causes impacts to the species now or is 
likely to cause impacts in the future. If there is exposure to a 
stressor and the species responds negatively, the stressor may be a 
threat. We consider the stressor to be a threat if it drives, or 
contributes to, the risk of extinction of the species such that the 
species warrants listing as endangered or threatened as those terms are 
defined in the Act. However, the identification of stressors that could 
affect a species negatively may not be sufficient to compel a finding 
that the species warrants listing. The information must include 
evidence sufficient to suggest that these stressors are operative 
threats that act on the species to the point that the species may meet 
the definition of endangered or threatened under the Act.
    Our species status report examines all of the potential stressors 
to iiwi in detail. Here we describe those stressors that we conclude 
rise to the level of a threat to the long-term viability of iiwi.
    Based on our comprehensive assessment of the status of the iiwi, we 
conclude that the best scientific data available consistently 
identifies avian malaria as the primary driver of declines in abundance 
and distribution of iiwi observed since the turn of the 20th century. 
This conclusion is supported by the extremely high mortality rate of 
iiwi (approximately 95 percent) in response to avian malaria, and the 
disappearance of iiwi from low-elevation ohia forest where it was 
formerly common and where malaria is prevalent today. Both the life 
cycle of the mosquito vector and the development and transmission of 
the malaria parasite are temperature-limited; thus, iiwi are now found 
primarily in high-elevation forests above 3,937 ft (1,200 m) where 
malaria prevalence and transmission is only brief and episodic, or 
nonexistent, under current conditions. The honeycreepers amakihi and 
apapane appear to be developing some resistance or tolerance to avian 
malaria (e.g., Woodworth et al. 2005, p. 1,531; Atkinson et al. 2014, 
p. 366; Samuel et al. 2015, pp. 12-13). In contrast, iiwi have not 
demonstrated any substantial sign of developing resistance to avian 
malaria to date and do not appear to be genetically predisposed to 
evolve resistance (Jarvi et al. 2004, pp. 2,164-2,166). As the 
prevalence of avian malaria increases in association with warmer 
temperatures (e.g., LaPointe et al. 2012, p. 217), the extent and 
impact of avian diseases upon iiwi are projected to become greatly 
exacerbated by climate change during this century.
    Additionally, on Hawaii Island, where 90 percent of the iiwi 
currently occur, the recently discovered tree disease, ohia wilt, 
commonly known in Hawaii as rapid ohia death (ROD), was identified as 
an emergent source of habitat loss and degradation that has the 
potential to exacerbate other stressors to ohia forest habitat, as well 
as reduce the amount of habitat remaining for iiwi in an already 
limited, disease-free zone contained within a narrow elevation band. 
Rapid ohia death leads to significant mortality of the ohia that iiwi 
depend upon for nesting and foraging. This disease is spreading rapidly 
and has become a matter of urgent concern. If ROD continues to spread 
across the native ohia forests, it will directly threaten iiwi by 
eliminating the limited, malaria-free native forest areas that remain 
for the species.
    Based on the analysis in our species status report, invasive, 
nonnative plants and feral ungulates have major, adverse impacts on 
ohia forest habitat. Although we did not find that the historical and 
ongoing habitat alteration by nonnative species is the primary cause of 
the significant observed decline in iiwi's abundance and distribution, 
the cumulative impacts to iiwi's habitat, and in particular the 
activities of feral ungulates, are not insignificant and likely 
exacerbate the effects of avian malaria. Feral ungulates, particularly 
pigs (Sus scrofa), goats (Capra hircus), and axis deer (Axis axis), 
degrade ohia forest habitat by spreading nonnative plant seeds and 
grazing on and trampling native vegetation, and contributing to erosion 
(Mountainspring 1986, p. 95; Camp et al. 2010, p. 198). Invasive 
nonnative plants, such as strawberry guava (Psidium cattleianum) and 
albizia trees (Falcataria moluccana), prevent or retard regeneration of 
ohia forest used by iiwi for foraging and nesting. The combined effects 
of drought and nonnative, invasive grasses have resulted in increased 
fire frequency and the conversion of mesic ohia woodland to exotic 
grassland in many areas of Hawaii ((D'Antonio and Vitousek 1992, p. 67; 
Smith and Tunison 1992, pp. 395-397; Vitousek et al. 1997, pp. 7-8; 
D'Antonio et al. 2011, p. 1,617). Beyond alteration of ohia forest, 
feral pig activities that create mosquito habitat in ohia forest where 
there would otherwise be very little to none is identified as an 
important compounding stressor that acts synergistically with the 
prevalence of malaria and results in iiwi mortality. Although habitat 
loss and degradation is not, by itself, considered to be a primary 
driver of iiwi declines, the habitat impacts described above contribute 
cumulatively to the vulnerability of the species to the threat of avian 
malaria by degrading the quality and quantity of the remaining disease-
free habitat upon which the iiwi depends. In this regard, ROD, 
discussed above, is a matter of urgent concern as it can further 
exacerbate and compound effects from the suite of stressors that impact 
iiwi (see below).

Avian Diseases

    The introduction of avian diseases transmitted by the introduced 
southern house mosquito (Culex quinquefasciatus), including avian 
malaria (caused by the protozoan Plasmodium relictum) and avian pox 
(Avipoxvirus sp.), has been a key driving force in both extinctions and 
extensive declines over the last century in the abundance, diversity, 
and distribution of many Hawaiian forest bird species, including 
declines of the iiwi and other endemic honeycreepers (e.g., Warner 
1968, entire; Van Riper et al. 1986, entire; Benning et al. 2002, p.

[[Page 43877]]

14,246; Atkinson and LaPointe 2009a, p. 243; Atkinson and LaPointe 
2009b, pp. 55-56; Samuel et al. 2011, p. 2,970; LaPointe et al. 2012, 
p. 214; Samuel et al. 2015, pp. 13-15). Nonnative to Hawaii, the first 
species of mosquitoes were accidentally introduced to the Hawaiian 
Islands in 1826, and spread quickly to the lowlands of all the major 
islands (Warner 1968, p. 104; Van Riper et al. 1986, p. 340). Early 
observations of birds with characteristic lesions suggest that avian 
pox virus was established in Hawaii by the late 1800s (Warner 1968, p. 
106; Atkinson and LaPointe 2009a, p. 55), and later genetic analyses 
indicate pox was present in the Hawaiian Islands by at least 1900 
(Jarvi et al. 2008, p. 339). Avian malaria had arrived in Hawaii in the 
early 20th century (Warner 1968, p. 107; Van Riper et al. 1986, pp. 
340-341; Atkinson and LaPointe 2009, p. 55; Banko and Banko 2009, p. 
52), likely in association with imported cage birds (Yorinks and 
Atkinson 2000, p. 731), or through the deliberate introduction of 
nonnative birds to replace the native birds that had by then 
disappeared from the lowlands (Atkinson and LaPointe 2009a, p. 55).

Avian Malaria

    As noted above, avian malaria is a disease caused by the protozoan 
parasite Plasmodium relictum; the parasite is transmitted by the 
mosquito Culex quinquefasciatus, and invades the red blood cells of 
birds. Birds suffering from malaria infection undergo an acute phase of 
the disease during which parasitemia, a quantitative measure of the 
number of Plasmodium parasites in the circulating red blood cells, 
increases steadily. Because the parasite destroys the red blood cells, 
anemia and decline of physical condition can quickly result. In native 
Hawaiian forest birds, death may result either directly from the 
effects of anemia, or indirectly when anemia-weakened birds become 
vulnerable to predation, starvation, or a combination of other 
stressors (LaPointe et al. 2012, p. 213). Native Hawaiian birds that 
survive avian malaria remain chronically infected, thus becoming 
lifetime reservoirs of the disease (Samuel et al. 2011, p. 2,960; 
LaPointe et al. 2012, p. 216) and remaining capable of further disease 
transmission to other native birds. In contrast, nonnative birds in 
Hawaii are little affected by avian malaria and later become incapable 
of disease transmission (LaPointe et al. 2012, p. 216).
    Wild iiwi infected with malaria are rarely captured, apparently 
because the onset of infection leads to rapid mortality, precluding 
their capture (Samuel et al. 2011, p. 2,967; LaPointe et al. 2016, p. 
11). However, controlled experiments with captive birds have 
demonstrated the susceptibility of native Hawaiian honeycreepers to 
avian malaria; mortality is extremely high in some species, including 
iiwi, experimentally infected with the disease. As early as the 1960s, 
experiments with Laysan finches (Telespiza cantans) and several other 
species of native Hawaiian honeycreepers demonstrated 100 percent 
mortality from malaria in a very short period of time (Warner 1968, pp. 
109-112, 118; Fig. 426).
    In a study specific to iiwi, Atkinson et al. (1995, entire) 
demonstrated that the species suffers approximately 95 percent 
mortality when infected with malaria (Atkinson et al. 1995, p. S65). 
All of the exposed iiwi developed infections within 4 days, with only a 
single male iiwi surviving. Following re-exposure with the same 
Plasmodium isolate after initial infection, no subsequent increase in 
parasitemia was detected, suggesting a possible development of some 
immunity (Atkinson et al. 1995, p. S66). The authors suggested that 
iiwi may lack sufficient diversity in the major histocompatibility 
complex or genetically based immunity traits capable of recognizing and 
responding to malarial antigens, an important factor in iiwi's 
susceptibility to introduced disease (Atkinson et al. 1995, pp. S65-
S66).
    Despite extremely high mortality of iiwi from avian malaria in 
general, the aforementioned study as well as two other studies have 
demonstrated that a few individuals have survived infection (Van Riper 
et al. 1986, p. 334; Atkinson et al. 1995, p. S63; Freed et al. 2005, 
p. 759). If a genetic correlation were identified, it is possible that 
surviving individuals could serve as a potential source for the 
evolution of genetic resistance to malaria, although evidence of this 
is scant to date. Eggert et al. (2008, p. 8) reported a slight but 
detectable level of genetic differentiation between iiwi populations 
located at mid and high elevation, potentially the first sign of 
selection acting on these populations in response to disease. 
Additionally, the infrequent but occasional sighting of iiwi on Oahu 
indicates a possible developed resistance or tolerance to avian 
malaria. Moreover, other more common honeycreepers, such as the amakihi 
and apapane, show signs of developing resistance or tolerance to the 
disease, as evidenced by molecular studies (e.g., Woodworth et al. 
2005, p. 1,531; Atkinson et al. 2014, p. 366) and their continued 
distribution at mid and low elevations where mosquitos and malaria 
transmission persist year-round (e.g., Foster et al. 2004, entire; 
Eggert et al. 2008, pp. 7-8).
    Despite these observations, there is no indication as of yet that 
iiwi have developed significant resistance to malaria such that 
individuals can survive in areas where the disease is strongly 
prevalent, including all potential low-elevation forest habitat and 
most mid-elevation forest habitat (Foster et al. 2007, p. 4,743; Eggert 
et al. 2008, p. 2). In one study, for example, 4 years of mist-netting 
effort across extensive areas of Hawaii Island resulted in the capture 
of a substantial number of iiwi, yet no iiwi were captured in low-
elevation forests and only a few were captured in mid-elevation forests 
(Samuel et al. 2015, p. 11). In addition, several studies indicate that 
iiwi have low genetic variability, and even genetic impediments to a 
possible evolved resistance to malaria in the future (Jarvi et al. 
2001, p. 255; Jarvi et al. 2004, Table 4, p. 2,164; Foster et al. 2007, 
p. 4,744; Samuel et al. 2015, pp. 12-13). For example, Eggert et al. 
(2008, p. 9) noted that gene variations that may confer resistance 
appear to be rare in iiwi.
    Three factors--the homogeneity of a portion of the iiwi genome, the 
high mortality rate of iiwi in response to avian malaria, and high 
levels of gene flow resulting from the wide-ranging nature of the 
species--suggest that iiwi would likely require a significant amount of 
time for development of genetic resistance to avian malaria, assuming 
the species retains a sufficiently large reservoir of genetic diversity 
for a response to natural selection. Genetic studies of iiwi have also 
noted a dichotomy between the lack of variation in mitochondrial DNA 
(Tarr and Fleischer 1993, 1995; Fleischer et al. 1998; Foster et al. 
2007, p. 4,743), and maintenance of variation in nuclear DNA (Jarvi et 
al. 2004, p. 2,166; Foster et al. 2007, p. 4,744); both attributes 
suggest that iiwi may have historically experienced a drastic reduction 
in population size that led to a genetic bottleneck. Studies have also 
found low diversity in the antigen-binding sites of the iiwi's major 
histocompatibility complex (that part of an organism's immune system 
that helps to recognize foreign or incompatible proteins (antigens) and 
trigger an immune response).
    The relationship between temperature and avian malaria is of 
extreme importance to the current persistence of iiwi and the viability 
of the species in the future. The development of the

[[Page 43878]]

Plasmodium parasite that carries malaria responds positively to 
increased temperature, such that malaria transmission is greatest in 
warm, low-elevation forests with an average temperature of 
72[emsp14][deg]F (22 [deg]C), and is largely absent in high-elevation 
forests above 4,921 ft (1,500 m) with cooler mean annual temperatures 
around 57[emsp14][deg]F (14 [deg]C) (Ahumada et al. 2004, p. 1,167; 
LaPointe et al. 2010, p. 318; Liao et al. 2015, p. 4,343). High-
elevation forests thus currently serve as disease-free habitat zones 
for Hawaiian forest birds, including iiwi. Once one of the most common 
birds in forests throughout the Hawaiian islands, iiwi are now rarely 
found at lower elevations, and are increasingly restricted to high-
elevation mesic and wet forests where cooler temperatures limit both 
the development of the malarial parasite and mosquito densities (Scott 
et al. 1986, pp. 367-368; Ahumada et al. 2004, p. 1,167; LaPointe et 
al. 2010, p. 318; Samuel et al. 2011, p. 2,960; Liao et al. 2015, p. 
4,346; Samuel et al. 2015, p. 14).
    Temperature also affects the life cycle of the malaria mosquito 
vector, Culex quinquefasciatus. Lower temperatures slow the development 
of larval stages and can affect the survival of adults (Ahumada et al. 
2005, pp. 1,165-1,168; LaPointe et al. 2012, p. 217). Although closely 
tied to altitude and a corresponding decrease in temperature, the 
actual range of mosquitoes varies with season. Generally, as 
temperature decreases with increasing elevation, mosquito abundance 
drops significantly at higher altitudes. In the Hawaiian Islands, the 
mosquito boundary occurs between 4,921 and 5,577 ft (1,500 and 1,700 m) 
(VanRiper et al. 1986, p. 338; LaPointe et al. 2012, p. 218). Areas 
above this elevation are at least seasonally relatively free of 
mosquitoes; thus, malaria transmission is unlikely at these high 
elevations under current conditions.
    Early on, Ralph and Fancy (1995, p. 741) and Atkinson et al. (1995, 
p. S66) suggested that the seasonal movements of iiwi to lower 
elevation areas where ohia is flowering may result in increased contact 
with malaria-infected mosquitoes, which, combined with the iiwi's high 
susceptibility to the disease, may explain their observed low annual 
survivorship relative to other native Hawaiian birds. Compounding the 
issue, other bird species that overlap with iiwi in habitat, including 
Apapane (Himatione sanguinea), are relatively resistant to the diseases 
and carry both Plasmodium and avian pox virus. As reservoirs, they 
carry these diseases upslope where mosquitoes are less abundant but 
still occur in numbers sufficient to facilitate and continue 
transmission to iiwi (Ralph and Fancy 1995, p. 741).
    Subsequent studies have confirmed the correlation between risk of 
malaria infection and iiwi altitudinal migrations, and suggest upper 
elevation forest reserves in Hawaii may not adequately protect mobile 
nectarivores such as iiwi. Kuntz (2008, p. 3) found iiwi populations at 
upper elevation study sites (6,300 ft (1,920 m)) declined during the 
non-breeding season when birds departed for lower elevations in search 
of flowering ohia, traveling up to 12 mi (19.4 km) over contiguous 
mosquito-infested wet forest. Guillamet et al. (2016, p. 192) used 
empirical measures of seasonal movement patterns in iiwi to model how 
movement across elevations increases the risk of disease exposure, even 
affecting breeding populations in disease-free areas. La Pointe et al. 
(unpublished data 2015) found that, based on malaria prevalence in all 
Hawaiian forest birds, species migrating between upper elevations to 
lower elevations increased their risk of exposure to avian malaria by 
as much as 27 times. The greater risk was shown to be due to a much 
higher abundance of mosquitoes at lower elevations, which in turn was 
attributable at least in part to the higher abundance of pigs and their 
activities in lower elevation forests (discussed further below).

Avian Pox

    Avian pox (or bird pox) is an infection caused by the virus 
Avipoxvirus, which produces large, granular, and eventually dead tissue 
lesions or tumors on exposed skin or infected lesions on the mouth, 
trachea, and esophagus of infected birds. Avian pox can be transmitted 
through cuts or wounds upon physical contact or through the mouth parts 
of blood-sucking insects such as the mosquito Culex quinquefasciatus, 
the common vector for both the pox virus and avian malaria (LaPointe et 
al. 2012, p. 221). Tumors or lesions caused by avian pox can be 
crippling for birds, and may result in death. Although not extensively 
studied, existing data suggest that mortality from avian pox may range 
from 4 to 10 percent observed in Oahu Elepaio (Chasiempis ibidis) (for 
birds with active lesions) (VanderWerf 2009, p. 743) to 100 percent in 
Laysan finches (Warner 1968, p. 108). VanderWerf (2009, p. 743) has 
also suggested that mortality levels from pox may correlate with higher 
rainfall years, and at least in the case of the Elepaio, observed 
mortality may decrease over time with a reduction in susceptible birds.
    As early as 1902, native birds suffering from avian pox were 
observed in the Hawaiian Islands, and Warner (1968, p. 106) described 
reports that epizootics of avian pox ``were so numerous and extreme 
that large numbers of diseased and badly debilitated birds could be 
observed in the field.'' As the initial wave of post-European 
extinctions of native Hawaiian birds was largely observed in the late 
1800s, prior to the introduction of avian malaria (Van Riper et al. 
1986, p. 342), it is possible that avian pox played a significant role, 
although there is no direct evidence (Warner 1968, p. 106). Molecular 
work has revealed two genetically distinct variants of the pox virus 
affecting forest birds in Hawaii that differ in virulence (Jarvi et al. 
2008, p. 347): One tends to produce fatal lesions, and the other 
appears to be less severe, based on the observation of recurring pox 
infections in birds with healed lesions (Atkinson et al. 2009, p. 56).
    The largest study of avian pox in scope and scale took place 
between 1977 and 1980, during which approximately 15,000 native and 
nonnative forest birds were captured and examined for pox virus lesions 
on Hawaii Island (Van Riper et al. 2002, pp. 929-942). The study made 
several important determinations, including that native forest birds 
were indeed more susceptible than introduced species, that all species 
were more likely to be infected during the wet season, and that pox 
prevalence was greatest at mid-elevation sites approximately 3,937 ft 
(1,200 m) in elevation, coinciding with the greatest overlap between 
birds and the mosquito vector. Of the 107 iiwi captured and examined 
during the study, 17 percent showed signs of either active or inactive 
pox lesions (Van Riper et al. 2002, p. 932). Many studies of avian pox 
have documented that native birds are frequently infected with both 
avian pox and avian malaria (Van Riper et al. 1986, p. 331; Atkinson et 
al. 2005, p. 537; Jarvi et al. 2008, p. 347). This may be due to 
mosquito transmission of both pathogens simultaneously, because 
documented immune system suppression by the pox virus renders 
chronically infected birds more vulnerable to infection by, or a 
relapse of, malaria (Jarvi et al. 2008, p. 347), or due to other 
unknown factors. The relative frequency with which the two diseases co-
occur makes it challenging to disentangle the independent impact of 
either stressor acting alone (LaPointe et al. 2012, p. 221). Although 
we lack

[[Page 43879]]

direct evidence of the degree to which pox may be a specific threat to 
iiwi or contributing to its decline, both field observations of and 
limited experimental studies on closely related species of 
honeycreepers suggests that it may be a significant factor (Warner 
1968, pp. 106, 108-109; VanRiper et al. 2002, pp. 936-939).

Compounded Impacts--Feral Ungulates Create Habitat for Culex 
Quinquefasciatus Mosquitoes and Exacerbate Impacts of Disease

    It has been widely established that damage to native tree ferns 
(Cibotium spp.) and rooting and wallowing activity by feral pigs create 
mosquito larval breeding sites in Hawaiian forests where they would not 
otherwise occur. The porous geology and relative absence of puddles, 
ponds, and slow-moving streams in most Hawaiian landscapes precludes an 
abundance of water-holding habitat sites for mosquito larvae; however, 
Culex quinquefasciatus mosquitoes, the sole vector for avian malaria in 
Hawaii, now occur in great density in many wet forests where their 
larvae primarily rely on habitats created by pig activity (LaPointe 
2006, pp. 1-3; Ahumada et al. 2009, p. 354; Atkinson and LaPointe 2009, 
p. 60; Samuel et al. 2011, p. 2,971). Pigs compact volcanic soils and 
create wallows and water containers within downed, hollowed-out tree 
ferns, knocked over and consumed for their starchy pith (Scott et al. 
1986, pp. 365-368; Atkinson et al. 1995, p. S68). The abundance of C. 
quinquefasciatus mosquitoes is also much greater in suburban and 
agricultural areas than in undisturbed native forest, and the mosquito 
is capable of dispersing up to 1 mile (1.6 kilometers) within closed-
canopy native forest, including habitat occupied by the iiwi (LaPointe 
2006, p. 3; LaPointe et al. 2009, p. 409).
    In studies of native forest plots where feral ungulates (including 
pigs) were removed by trapping and other methods, researchers have 
demonstrated a correlation in the abundance of Culex spp. mosquitoes 
when comparing pig-free, fenced areas to adjacent sites where feral pig 
activity is unmanaged. Aruch et al. 2007 (p. 574), LaPointe 2006 (pp. 
1-3) and LaPointe et al. (2009, p. 409; 2012, pp. 215, 219) assert that 
management of feral pigs may be strategic to managing avian malaria and 
pox, particularly in remote Hawaiian rain forests where studies have 
documented that habitats created by pigs are the most abundant and 
productive habitat for larval mosquitoes. Reduction in mosquito habitat 
must involve pig management across large landscapes due to the 
tremendous dispersal ability of C. quinquefasciatus and the possibility 
of the species invading from adjacent areas lacking management 
(LaPointe 2006, pp. 3-4). The consequences of feral pig activities thus 
further exacerbate the impacts to iiwi from avian malaria and avian 
pox, by creating and enhancing larval habitats for the mosquito vector, 
thereby increasing exposure to these diseases.

Avian Diseases--Summary

    The relatively recent introduction of avian pox and avian malaria, 
in concert with the introduction of the mosquito disease vector, is 
widely viewed as one of the key factors underlying the loss and decline 
of native forest birds throughout the Hawaiian Islands. Evolving in the 
absence of mosquitoes and their vectored pathogens, native Hawaiian 
forest birds, particularly honeycreepers such as iiwi, lack natural 
immunity or genetic resistance, and thus are more susceptible to these 
diseases than are nonnative bird species (van Riper et al. 1986, pp. 
327-328; Yorinks and Atkinson 2000, p. 737). Researchers consider iiwi 
one of the most vulnerable species, with an average of 95 percent 
mortality in response to infection with avian malaria (Atkinson et al. 
1995, p. S63; Samuel et al. 2015, p. 2).
    Many native forest birds, including iiwi, are now absent from warm, 
low-elevation areas that support large populations of disease-carrying 
mosquitoes, and these birds persist only in relatively disease-free 
zones in high-elevation forests, above roughly 4,921 to 5,577 ft (1,500 
to 1,700 m), where both the development of the malarial parasite and 
the density of mosquito populations are held in check by cooler 
temperatures (Scott et al. 1986, pp. 85, 100, 365-368; Woodworth et al. 
2009, p. 1,531; Liao et al. 2015, pp. 4,342-4,343; Samuel et al. 2015, 
pp. 11-12). Even at these elevations, however, disease transmission may 
occur when iiwi move downslope to forage on ephemeral patches of 
flowering ohia in the nonbreeding season, encountering disease-carrying 
mosquitoes in the process (Ralph and Fancy 1995, p. 741; Fancy and 
Ralph 1998, p. 3; Guillaumet et al. 2015, p. EV-8; LaPointe et al. 
2015, p. 1). Iiwi have not demonstrably developed resistance to avian 
malaria, unlike related honeycreepers including Amakihi (Hemignathus 
spp.) and Apapane. Due to the extreme mortality rate of iiwi when 
exposed to avian malaria, we consider avian malaria in particular to 
pose a threat to iiwi. Having already experienced local extinctions and 
widespread population declines, it is possible that the species may not 
possess sufficient genetic diversity to adapt to these diseases 
(Atkinson et al. 2009, p. 58).

Climate Change

    Based on the assessment of the best scientific data available, we 
conclude that climate change exacerbates the impacts to iiwi from 
mosquito-borne disease, and this effect is likely to continue and 
worsen in the future. Air temperature in Hawaii has increased in the 
past century and particularly since the 1970s, with the greatest 
increases at higher elevations, and several conservative climate change 
models project continued warming in Hawaii into the future. As a 
result, the temperature barrier to the development and transmission of 
avian malaria will continue to move up in elevation in response to 
warmer conditions, leading to the curtailment or loss of disease-free 
habitats for iiwi. We briefly discuss below three climate studies that 
conservatively predict the iiwi will lose between 60 and 90 percent of 
its current (and already limited) disease-free range by the end of this 
century, with significant effects occurring by mid-century.

Climate Change Effects on Iiwi

    Climate change is a stressor that is likely to significantly 
exacerbate the effects of avian malaria on iiwi both directly through 
increased prevalence and mortality, and indirectly through the loss of 
disease-free habitat. Air temperature in Hawaii has increased in the 
past century and particularly since the 1970s, with greater increases 
at high elevation (Giambelluca et al. 2008, pp. 2-4; Wang et al. 2014, 
pp. 95, 97). Documented impacts of increased temperature include the 
prevalence of avian malaria in forest birds at increasing elevation, 
including high-elevation sites where iiwi are already declining, for 
example, on Kauai (Paxton et al. 2013, p. 13; Paxton et al. 2016, 
entire). Several projections for future climate in Hawaii describe a 
continued warming trend, especially at high elevations. In our species 
status report, we analyzed in particular three climate studies 
(summarized below) that address the future of native forest birds, 
including iiwi, in the face of the interactions between climate change 
and avian malaria.
    Benning et al. (2002) concluded that under optimistic assumptions 
(i.e., 3.6 [deg]F (2 [deg]C) increase in temperature by the year 2100), 
malaria-susceptible Hawaiian forest birds, including iiwi, will lose 
most of their disease-free habitat in the three sites they considered

[[Page 43880]]

in their projection of climate change impacts. For example, current 
disease-free habitat at high elevation within the Hakalau Forest 
National Wildlife Refuge (NWR) on the island of Hawaii (where the 
environment is still too cold for development of the malarial parasite) 
would be reduced by 96 percent by the end of the century.
    Fortini et al. (2015) conducted a vulnerability assessment for 20 
species of Hawaiian forest birds based on a projected increase of 6.1 
[deg]F (3.4 [deg]C) under the A1B emissions scenario at higher 
elevations by 2100. Even under this relatively optimistic scenario, in 
which emissions decline after mid-century (IPCC 2007, p. 44), all 
species were projected to suffer range loss as the result of increased 
transmission of avian malaria at higher elevations with increasing 
temperature. Iiwi was predicted to lose 60 percent of its current range 
by the year 2100, and climate conditions suitable for the species will 
shift up in elevation, including into areas that are not currently 
forested, such as lava flows and high-elevation grasslands. Most of the 
remaining habitat for iiwi would be restricted to a single island, 
Hawaii Island.
    Liao et al. (2015) generated temperature and precipitation 
projections under three alternative emissions scenarios and projected 
future malaria risk for Hawaiian forest birds. Irrespective of the 
scenario modeled, by mid-century (roughly 2040), malaria transmission 
rates and impacts to bird populations began increasing at high 
elevations. By 2100, the increased annual malaria transmission rate for 
iiwi was projected to result in population declines of 70 to 90 percent 
for the species, depending on the emissions scenario.
    All three of these studies consistently predict a significant loss 
of disease-free habitat for iiwi with consequent severe reductions in 
population size and distribution by the year 2100, with significant 
changes likely to be observed as early as 2040. As the iiwi's numbers 
and distribution continue to decline, the remaining small, isolated 
populations become increasingly vulnerable to loss of ohia forest 
habitat from other stressors such as ROD, as well as other 
environmental catastrophes and demographic stochasticity, particularly 
should all remaining iiwi become restricted to a single island (Hawaii 
Island), as some scenarios suggest.
    Climate change will likely exacerbate other stressors to iiwi in 
addition to disease. Projected increases in temperature and humidity 
are likely to increase the spatial extent of areas on Hawaii Island 
vulnerable to ROD (Keith 2016, pers. comm). Changes in the amount and 
distribution of rainfall in Hawaii likely will affect the quality and 
extent of mesic and wet forests on which iiwi depend. Hawaii has 
experienced an overall drying trend since the 1920s, with an average 
annual decline in precipitation of 1.78 percent (Frazier and 
Giambelluca 2016, p. 4), but some future projections suggest that areas 
that currently are wet (windward sides of islands) will experience 
greater rainfall and more extreme rainfall events, while currently dry 
areas (leeward sides and high elevations) will become drier (Zhang et 
al. 2016, pp. 8,350-8,351). Changes in the trade wind inversion (which 
strongly influences rainfall) and other aspects of precipitation with 
climate change are difficult to model with confidence, complicating 
projections of future precipitation in Hawaii on various spatial scales 
(Chu and Chen 2005, pp. 4,801-4,802; Cao et al. 2007, pp. 1,158-1,159; 
Timm et al. 2015, p. 107; Fortini et al. 2015, p. 5; Liao et al. 2015, 
p. 4,345). In addition, potential increases in storm frequency and 
intensity in Hawaii as a result of climate change may lead to an 
increase in direct mortality of individual iiwi and a decline in the 
species' reproductive success. Currently, no well-developed projections 
exist for these possible cumulative effects.

Climate Change--Summary

    The natural susceptibility of native forest birds to introduced 
diseases, in combination with the observed restriction of Hawaiian 
honeycreepers to high-elevation forests, led Atkinson et al. (1995, p. 
S68) to predict two decades ago that a shift in the current mosquito 
distribution to higher elevations could be ``disastrous for those 
species with already reduced populations.'' Thus, climate change has 
significant implications for the future of Hawaiian forest birds, as 
predictions suggest increased temperatures may largely eliminate the 
high-elevation forest currently inhospitable to the transmission of 
mosquito-borne diseases (Benning et al. 2002, pp. 14,247-14,249; 
LaPointe et al. 2012, p. 219; Fortini et al. 2015, p. 9). Samuel et al. 
(2015, p. 15) predict further reductions and extinctions of native 
Hawaiian birds as a consequence, noting that the iiwi is particularly 
vulnerable due to its high susceptibility to malaria. Finally, Paxton 
et al. (2016, entire) report a steepening decline in iiwi and other 
honeycreepers on Kauai since 2000.
    Iiwi is projected to be extirpated from Kauai by 2050 as a result 
of the island having now passed a ``tipping point'' where increasing 
temperature exposes birds to mosquito-borne disease throughout their 
remaining range on the island; if the current trends of decline in 
distribution and abundance continue in a linear fashion in the future, 
iiwi could be extirpated from Kauai much sooner (Paxton et al. 2016, 
pp. 3, 5). The maximum elevation of forest habitat on Kauai (about 
4,900 ft (1,500 m)) is less than that on either Maui or Hawaii Island, 
where similar trends of increase in temperature and the elevation of 
disease transmission are well documented, as discussed above. Iiwi, and 
other disease-susceptible honeycreepers, only persist in abundance on 
these higher islands in high-elevation, disease-free habitat that is 
shrinking with increasing temperature. In sum, several independent 
studies project consistently significant negative impacts to the iiwi 
as a result of climate change and the increased exposure to avian 
malaria as disease-free habitats shrink. As iiwi are known to exhibit 
95 percent mortality on average as a result of avian malaria, the 
current numbers of iiwi are of little consequence should all or most of 
the remaining individuals become exposed to the disease in the future.

Rapid Ohia Death

    Rapid ohia death, a new disease that kills ohia trees, is a factor 
with the potential to exacerbate the threats currently affecting iiwi 
and reduce the amount of disease-free habitat remaining by destroying 
high-elevation ohia forest. Unexplained, widespread mortality of ohia 
trees was first detected in 2012 in lowland forests of the Puna Region 
of Hawaii Island (Keith et al. 2015, entire). Pathogenicity tests 
conducted by the USDA Agriculture Research Service determined that the 
vascular wilt disease, now commonly known in Hawaii as rapid ohia death 
(ROD), is caused by the fungus Ceratocystis fimbriata (Keith et al. 
2015, pp. 1-2). A second, new species of Ceratocystis also kills ohia; 
this new species is being described as of this writing (Hughes 2016, 
pers. comm.; Keith 2016, pers. comm.).
    Ohia stands experience rapid and extensive mortality from ROD. In 
2014, approximately 15,000 ac (6,000 ha) of ohia forest from Kalapana 
to Hilo on Hawaii Island experienced greater than 50 percent mortality, 
with 100 percent mortality in some stands over a two to three year 
period (Friday et al. 2015, p. 1). Between 2014 and 2015, annual 
mortality rates measured in monitoring plots averaged from 24 percent 
(measured as ohia stems) to 28 percent

[[Page 43881]]

(measured as ohia basal area) (Mortenson et al. 2016, p. 89). When 
these plots were established in the ROD-infected area in January and 
February of 2014, all had already experienced an average of 
approximately 39 percent ohia mortality (Mortenson et al. 2016, p. 89).
    At present, the disease remains restricted to Hawaii Island, where 
it is spreading rapidly. In 2016, the amount of forest area affected on 
Hawaii Island was estimated to be more than 50,000 ac (20,235 ha), and 
this estimate includes a new outbreak in Laupahoehoe Forest Reserve on 
the Hamakua Coast (Hughes 2016, pers. comm.). The largest affected area 
is within the Puna District, where infected trees have been observed 
within approximately 4,000 discontinuous acres (1,619 ha) (Hughes 2016, 
pers. comm.). In some areas, dead and dying trees affected by the 
fungus have been observed within the range of iiwi (Hughes 2016, pers. 
comm.; Keith 2016, pers. comm.). Affected trees are found at elevations 
ranging from sea level up to approximately 5,000 ft (1,524 m), 
including at Wailuku Forest near Hakalau Forest NWR (Hughes 2016, pers. 
comm.), which contains a stable to increasing iiwi population (Paxton 
et al. 2013, p. 12). Hawaii Island is home to 90 percent of the current 
iiwi population, and this island will remain particularly important for 
the species: Iiwi are predicted to be largely if not entirely 
restricted to that island under some future climate change projections 
(Fortini et al. 2015, p. 9, Supplement 6).

Evaluation of Existing Regulatory Mechanisms and Conservation Measures

    Our species status report evaluated several regulatory and other 
measures in place today that might address or are otherwise intended to 
ameliorate the stressors to iiwi. Our analysis concluded that forest 
habitat protection, conservation, and restoration has the potential to 
benefit iiwi by protecting and enhancing breeding and foraging areas 
for the species while simultaneously reducing the abundance of mosquito 
breeding sites, despite the disease vector's (Culex quinquefasciatus) 
1-mi (1.6-km) dispersal ability (LaPointe et al. 2009, pp. 408; 411-
412; LaPointe et al. 2012, p. 215).
    Because of the iiwi's extreme susceptibility to avian malaria, 
habitat to sustain the species must be disease-free. Efforts to restore 
and manage large, contiguous tracts of native forests have been shown 
to benefit iiwi, especially when combined with fencing and ungulate 
removal (LaPointe et al. 2009, p. 412; LaPointe et al. 2012, p. 219). 
While forest restoration and ungulate management at the Hakalau Forest 
NWR on Hawaii Island are excellent examples of what is needed to 
increase iiwi abundance, many similar large-scale projects would be 
necessary rangewide to simply reduce mosquito abundance and protect the 
species from current habitat threats alone. However, even wide-scale 
landscape habitat management would be unable to fully address the 
present scope of the threat of disease, and sufficient high-elevation 
forest is not available to provide disease-free habitat for iiwi in the 
face of future climate change. Even if disease-free habitat within 
managed areas could be restored and protected now, much of this habitat 
will lose its disease-free status as avian malaria moves upward in 
elevation in response to warming temperatures, as is occurring already 
within the Alakai Wilderness on the island of Kauai.
    New opportunities are emerging, such as large-scale vector control 
using new tools that have the potential to assist Hawaiian forest birds 
(LaPointe et al. 2009, pp. 416-417; Reeves et al. 2014, p. e97557; 
Gantz et al. 2015, pp. E6736-E6743; Fischer in press, pp. 1-2). The 
most promising of these new tools forego chemicals as a means of lethal 
control and directly manipulate the viability (or fitness) of the 
mosquitoes and can be grouped into tw