Endangered and Threatened Wildlife and Plants; Threatened Species Status for the Iiwi (Drepanis coccinea)
Federal Register, Volume 81 Issue 182 (Tuesday, September 20, 2016)
Federal Register Volume 81, Number 182 (Tuesday, September 20, 2016)
Proposed Rules
Pages 64414-64426
From the Federal Register Online via the Government Publishing Office www.gpo.gov
FR Doc No: 2016-22592
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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: 12-Month petition finding; proposed rule.
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SUMMARY: We, the U.S. Fish and Wildlife Service (Service), announce a 12-month finding on a petition to list the iiwi (Drepanis coccinea), a bird species from the Hawaiian Islands, as a threatened species under the Endangered Species Act (Act). After review of all best available scientific and commercial information, we find that listing the iiwi as a threatened species under the Act is warranted. Accordingly, we propose to list the iiwi as a threatened species throughout its range. If we finalize this rule as proposed, it would extend the Act's protections to this species. The effect of this regulation will be to add this species to the Federal List of Endangered and Threatened Wildlife.
DATES: We will accept comments received or postmarked on or before November 21, 2016. Comments submitted electronically using the Federal eRulemaking Portal (see ADDRESSES below) must be received by 11:59 p.m. Eastern Time on the closing date. We must receive requests for public hearings, in writing, at the address shown in FOR FURTHER INFORMATION CONTACT by November 4, 2016.
ADDRESSES: You may submit comments by one of the following methods:
(1) Electronically: Go to the Federal eRulemaking Portal: http://www.regulations.gov. In the Search box, enter FWS-R1-ES-2016-0057, which is the docket number for this rulemaking. Then, in the Search panel on the left side of the screen, under the Document Type heading, click on the Proposed Rules link to locate this document. You may submit a comment by clicking on ``Comment Now!''
(2) By hard copy: Submit by U.S. mail or hand-delivery to: Public Comments Processing, Attn: FWS-R1-ES-2016-0057; U.S. Fish and Wildlife Service Headquarters, MS: BPHC, 5275 Leesburg Pike, Falls Church, VA 22041-3803.
We request that you send comments only by the methods described above. We will post all comments on http://www.regulations.gov. This generally means that we will post any personal information you provide us (see Public Comments below for more information).
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 Information Relay Service (FIRS) at 800-877-
8339.
SUPPLEMENTARY INFORMATION: This document consists of: (1) A 12-month petition finding that listing the iiwi under the Act is warranted; and (2) a proposed rule to list the iiwi as a threatened species under the Act.
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.
We are proposing to list 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 proposes the listing of the iiwi as a threatened species. We previously published a 90-day finding for the iiwi, and this document includes a 12-month finding and proposed listing rule, which assesses 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 disease that affects 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.
We will seek peer review. We will seek comments from independent specialists to ensure that our designation is based on scientifically sound data, assumptions, and analyses. We will invite these peer reviewers to comment on our listing proposal. Because we will consider all comments and information received during the comment period, our final determination may differ from this proposal.
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
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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. We will invite at least three scientists with expertise in Hawaiian forest bird biology, avian malaria, and climate change to conduct an independent peer review of the species status report. The species status report and other materials relating to this proposal can be found at http://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).
Information Requested
Public Comments
We intend that any final action resulting from this proposed rule will be based on the best scientific and commercial data available and be as accurate and as effective as possible. Therefore, we request comments or information from the public, including land owners and land managers, other concerned governmental agencies, the scientific community, industry, or any other interested parties concerning this proposed rule. We particularly seek comments concerning:
(1) The iiwi's biology, range, and population trends, including:
(a) Biological or ecological requirements of the species, including habitat requirements for feeding, breeding, and sheltering;
(b) Genetics and taxonomy;
(c) Historical and current range including distribution patterns;
(d) Historical and current population levels, and current and projected trends; and
(e) Past and ongoing conservation measures for the species, its habitat, or both.
(2) Factors that may affect the continued existence of the species, which may include habitat modification or destruction, overutilization, disease, predation, the inadequacy of existing regulatory mechanisms, or other natural or manmade factors.
(3) Biological, commercial trade, or other relevant data concerning any threats (or lack thereof) to this species and existing regulations that may be addressing those threats.
(4) Additional information concerning the historical and current status, range, distribution, and population size of this species, including the locations of any additional populations of the iiwi.
(5) Specific information on:
What areas currently occupied, and that contain the necessary physical or biological features essential for the conservation of the iiwi, we should include in any future designation of critical habitat and why;
Whether special management considerations or protections may be required for the physical or biological features essential to the conservation of the iiwi; and
What areas not currently occupied are essential to the conservation of the iiwi and why.
Please include sufficient information with your submission (such as scientific journal articles or other publications) to allow us to verify any scientific or commercial information you include.
Please note that submissions merely stating support for or opposition to the action under consideration without providing supporting information, although noted, will not be considered in making a determination, as section 4(b)(1)(A) of the Act directs that determinations as to whether any species is a threatened or endangered species must be made ``solely on the basis of the best scientific and commercial data available.''
You may submit your comments and materials concerning this proposed rule by one of the methods listed in ADDRESSES. We request that you send comments only by the methods described in ADDRESSES.
If you submit information via http://www.regulations.gov, your entire submission--including any personal identifying information--will be posted on the Web site. If your submission is made via a hardcopy that includes personal identifying information, you may request at the top of your document that we withhold this information from public review. However, we cannot guarantee that we will be able to do so. We will post all hardcopy submissions on http://www.regulations.gov.
Comments and materials we receive, as well as supporting documentation we used in preparing this proposed rule, will be available for public inspection on http://www.regulations.gov, or by appointment, during normal business hours, at the U.S. Fish and Wildlife Service, Pacific Islands Fish and Wildlife Office (see FOR FURTHER INFORMATION CONTACT).
Public Hearing
Section 4(b)(5) of the Act provides for one or more public hearings on this proposal, if requested. Requests must be received within 45 days after the date of publication of this proposed rule in the Federal Register. Such requests must be sent to the address shown in FOR FURTHER INFORMATION CONTACT. We will schedule one or more public hearings on this proposal, if any are requested, and announce the dates, times, and places of those hearings, as well as how to obtain reasonable accommodations, in the Federal Register and local newspapers at least 15 days before the hearing.
Peer Review
In accordance with our joint policy on peer review published in the Federal Register on July 1, 1994 (59 FR 34270), we will seek the expert opinions of appropriate and independent specialists regarding this proposed rule and the accompanying draft species status report (see Status Assessment for the Iiwi, below). The purpose of peer review is to ensure that our listing determination is based on scientifically sound data, assumptions, and analyses. Peer reviewers have expertise in the iiwi's life history, habitat, physical and biological requirements, avian diseases including malaria, and climate change, and are currently reviewing the draft species status report, which will inform our determination. We invite comment from the peer reviewers during this public comment period.
Background
Section 4(b)(3)(B) of the Act requires that, for any petition to revise the Federal Lists of Threatened and Endangered Wildlife and Plants (Lists) that contains substantial scientific or commercial information indicating that listing a species may be warranted, we make a finding within 12 months of the date of receipt of the petition that the petitioned action is either: (a) Not warranted; (b) warranted; or (3) warranted, but the immediate proposal of a regulation implementing the petitioned action is precluded by pending proposals to determine whether other species are endangered or threatened, and expeditious progress is being made to add or remove qualified species from the Lists. With this publication, we have determined that the petitioned action to list the iiwi is warranted, and we are proposing to list the species.
Previous Federal Actions
On August 25, 2010, we received a petition dated August 24, 2010, from Noah Greenwald, Center for Biological Diversity, and Dr. Tony Povilitis, Life Net, requesting that the iiwi be listed as an endangered or threatened species and that critical habitat be designated under the Act. In a September 10, 2010, letter to the petitioners, we responded
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that we had reviewed the information presented in the petition and determined that issuing an emergency regulation temporarily listing the species under section 4(b)(7) of the Act was not warranted. We also stated that we were required to complete a significant number of listing and critical habitat actions in Fiscal Year 2010, including complying with court orders and court-approved settlement agreements with specific deadlines, listing actions with absolute statutory deadlines, and high-priority listing actions. Our listing and critical habitat funding for Fiscal Year 2010 was committed to complying with these court orders, settlement agreements, and statutory deadlines. Therefore, we were unable to further address the petition to list the iiwi at that time.
We published a 90-day finding for the iiwi in the Federal Register on January 24, 2012 (77 FR 3423). Based on that review, we found that the petition presented substantial information indicating that listing the iiwi may be warranted, and we initiated a status review of the species. With the publication of this notice, we provide our 12-month finding and a proposal to list the iiwi as a threatened species under the Act.
Status Assessment for the Iiwi
A thorough review of the taxonomy, life history, and ecology of the iiwi (Drepanis coccinea) is presented in the draft Iiwi (Drepanis coccinea) Species Status Report, available online at http://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 proposed for listing as a threatened or endangered species under the Act. It does, however, provide the scientific basis that informs our regulatory decision, which involves the further application of standards within the Act and its implementing regulations and policies. 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 (Hawaii Audubon Society 2011, p. 97), 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 (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 (Pratt et al. 2009, p. 193; Hawaii Audubon Society 2011, p. 97).
Although iiwi may breed anytime between October and August (Hawaii Audubon Society 2011, p. 97), 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 (Hawaii Audubon Society 2011, p. 97), 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 (Hawaii Audubon Society 2011, p. 97).
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. 2015, pp. EV-8--EV-9). 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).
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 2,551 birds (range 1,934 to 3,167) (Paxton et al. 2013, p. 10). 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), there is evidence for stable or declining populations on the windward side of the island, while trends are strongly increasing on the leeward (Kona) side. 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 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 draft 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
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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, ohia rust, drought, fires, volcanic eruptions, climate change, and particularly rapid ohia death 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 in our species status report, 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. 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 disease rapid ohia death 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, a recently discovered tree disease that leads to significant mortality of the ohia that iiwi depend upon for nesting and foraging, is quickly becoming a matter of urgent concern. If rapid ohia death 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, rapid ohia death, discussed above, is quickly becoming 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. 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 poxvirus 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 by at least 1920 (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
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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). Studies have demonstrated that 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). In that study, iiwi and a nonnative control species were exposed to avian malaria through infective mosquito bites, and subjected to different dosages of infection (single vs. multiple bites). Following exposure to biting mosquitoes, food consumption, weight, and parasitemia were monitored for all test groups. None of the nonnative birds developed malarial infections, while all of the exposed iiwi developed infections within 4 days. Mortality of the high-dose iiwi reached 100 percent by day 29, and mortality of the low-dose birds reached 90 percent by day 37, an average of 95 percent mortality between the two groups (Atkinson et al. 1994, p. S63). A single male iiwi survived the initial infection and, following re-exposure with the same Plasmodium isolate, 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 are capable of surviving the 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.
Despite these observations, there is, as of yet, no indication 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, the results of 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 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 72emsp14degF (22 degC), and is largely absent in high-elevation forests above 4,921 ft (1,500 m) with cooler mean annual temperatures around 57emsp14degF (14 degC) (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.
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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, which 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. (2015, 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 necrotic lesions or tumors on exposed skin or diphtheritic 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 from 16 different locations on transects along Mauna Loa 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), and we lack any indication of the degree to which pox may be a specific threat to iiwi or contributing to its decline.
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;
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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. Studies suggest that 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 studies showing 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 known 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 in our species status report, we concluded 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). 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 degF (2 degC) 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 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 degF (3.4 degC) 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
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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 rapid ohia death, 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. 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. However, changes in the trade wind inversion (which strongly influences rainfall) and other aspects of precipitation with climate change are difficult to model with confidence (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. 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
Our species status report identified rapid ohia death (ROD), a type of Ceratosystis spp. vascular wilt (fungal) disease, as a factor with the potential to exacerbate the impacts currently affecting iiwi habitat and reduce the amount of disease-free habitat remaining by destroying high-elevation ohia forest. ROD was first detected in 2012 as ohia trees began mysteriously dying within lowland forests of the Puna Region of Hawaii Island. In June 2015, researchers identified the disease as ROD with an estimated area at the time of 15,000 ac (6,070 ha) of infected ohia trees (Keith et al. 2015, pp. 1-2). ROD affects non-contiguous ohia forest stands ranging in size from
