                                   PUBLISHED

                    UNITED STATES COURT OF APPEALS
                        FOR THE FOURTH CIRCUIT


                                    No. 16-1457


PEGGY HILL; AMY WALKER,

                  Plaintiffs - Appellants,

            v.

BARRY COGGINS, d/b/a Cherokee Bear Zoo; COLLETTE COGGINS, d/b/a
Cherokee Bear Zoo,

                 Defendants - Appellees.
________________________

THE HUMANE SOCIETY OF THE UNITED STATES; THE FUND FOR
ANIMALS,

                  Amici Supporting Appellant.


                                    No. 16-1477


PEGGY HILL; AMY WALKER,

                  Plaintiffs - Appellees,

            v.

BARRY COGGINS, d/b/a Cherokee Bear Zoo; COLLETTE COGGINS, d/b/a
Cherokee Bear Zoo,

                 Defendants - Appellants.
________________________
THE HUMANE SOCIETY OF THE UNITED STATES; THE FUND FOR
ANIMALS,

                    Amici Supporting Appellee.


Appeals from the United States District Court for the Western District of North Carolina,
at Bryson City. Martin K. Reidinger, District Judge. (2:13-cv-00047-MR-DLH)


Argued: March 24, 2017                                        Decided: August 14. 2017


Before FLOYD and HARRIS, Circuit Judges, and John Preston BAILEY, United States
District Judge for the Northern District of West Virginia, sitting by designation.


Affirmed in part, vacated in part, and remanded by published opinion. Judge Floyd wrote
the opinion in which Judge Harris joined. Judge Bailey wrote a separate opinion
concurring in part and dissenting in part.


ARGUED: James S. Whitlock, DAVIS & WHITLOCK, P.C., Asheville, North
Carolina, for Appellants/Cross-Appellees. Mark R. Melrose, MELROSE LAW, PLLC,
Waynesvile, North Carolina, for Appellees/Cross-Appellants. ON BRIEF: Douglas A.
Ruley, DAVIS & WHITLOCK, P.C., Asheville, North Carolina, for Appellants/Cross-
Appellees. Anna Frostic, THE HUMANE SOCIETY OF THE UNITED STATES,
Washington, D.C., for Amici Curiae.




                                           2
FLOYD, Circuit Judge:

       Defendants Barry Coggins and Collette Coggins, doing business as the Cherokee

Bear Zoo (collectively, “the Zoo”), keep, care for, and exhibit bears. In 2013, Plaintiffs

Peggy Hill and Amy Walker (collectively, “Plaintiffs”) visited the Zoo, and observed

four of the Zoo’s bears living in what Plaintiffs believed to be an inhumane setting. In

response, Plaintiffs brought the instant suit against the Zoo, claiming that the Zoo’s

allegedly poor maintenance of its bears constitutes an unlawful taking proscribed by the

Endangered Species Act (ESA), 16 U.S.C. § 1538 et seq.

       The district court approved of Plaintiffs’ standing to bring their suit, and found

that the four subject bears were grizzly bears protected by the ESA.              The court

nonetheless concluded that the manner in which the Zoo maintains its bears—although

“archaic,” Hill v. Coggins, No. 2:13-cv-47, 2016 WL 1251190, at *14 (W.D.N.C. Mar.

30, 2016)—does not amount to an unlawful taking.

       For the reasons that follow, we affirm the district court’s rulings in favor of

Plaintiffs on the issues of standing and the subject bears’ status as protected grizzly bears.

We conclude, however, that the court’s ruling against Plaintiffs on the issue of whether

the Zoo is committing an unlawful taking was premised on incorrect legal analysis. We

therefore vacate that ruling and remand this case for further proceedings.


                                              I.

       Plaintiffs reside within the Qualla Boundary in Cherokee, North Carolina.

Plaintiffs are members of the Eastern Band of Cherokee Indians (“EBCI”). Like many


                                              3
members of the EBCI, Plaintiffs possess a deep cultural and spiritual connection with

wildlife, including bears.

       On March 28, 2013, Plaintiffs visited the Zoo. Plaintiffs observed a sign on the

Zoo’s premises advertising grizzly bears; they then proceeded to two bear pits containing

four bears, at least three of which were identified by nearby signs as grizzly bears. The

pits were compact and made entirely of concrete. Each pit had a small pool of water, but

neither had any vegetation nor any shade.

       Plaintiffs observed the bears in listless form, pacing around in their pits. They also

witnessed the bears begging for food, with patrons responding by feeding the bears

apples and dry bread sold by the Zoo.

       Ms. Hill observed the bears for a period of approximately thirty minutes, while

Ms. Walker observed the bears for a period of fifteen to twenty minutes. Plaintiffs claim

to have left feeling angry and upset with what they observed at the Zoo. Plaintiffs refuse

to return to the Zoo while the bears are in their current living conditions, but they have

expressed a desire to return if those conditions are improved.

       After their encounter with the bears, Plaintiffs brought this citizen suit against the

Zoo in federal district court. Plaintiffs alleged that the Zoo’s practice of keeping four

(apparent) grizzly bears in the above-described living conditions constitutes a “tak[ing]”

of a threatened species proscribed by 16 U.S.C. § 1538(a)(1)(B), and possession of a

“taken,” threatened species proscribed by 16 U.S.C. § 1538(a)(1)(D). The basis for these

allegations was Plaintiffs’ view that the Zoo’s conduct is a form of “harass[ment]” of,

and “harm” to, its bears. See 16 U.S.C. § 1532(19) (defining “take” as, inter alia, “to

                                             4
harass” or “harm”). Plaintiffs sought injunctive relief in response to the Zoo’s alleged

violations of the ESA.

       The Zoo filed a motion to dismiss Plaintiffs’ suit, which the district court denied

on June 17, 2014. The Zoo subsequently filed a motion for summary judgment, which

the district court denied on August 13, 2015. As a result, on September 17 and 18, 2015,

the parties participated in a bench trial. At trial, Plaintiffs gave testimony describing their

observations of the bears, their corresponding reactions, and their desires to observe the

bears living in humane conditions.

       Plaintiffs also presented extensive evidence demonstrating that the subject bears

are grizzly bears.    This evidence includes exhibits of the Zoo’s webpage, entitled

“Grizzlies Page,” J.A. 673–74, which identified the four bears as grizzly bears; signs at

the Zoo’s facility identifying at least three of the four bears as grizzly bears; veterinary

records identifying the four bears as grizzly bears; and United States Department of

Agriculture (USDA) reports identifying at least some of the bears as grizzly bears.

Additionally, Edward Ramsay, D.V.M.—one of Plaintiffs’ expert witnesses and a

diplomate of the American College of Zoological Medicine—identified the subject bears

as grizzly bears based on his observation of distinctive shoulder humps on the bears. 1


       1
         Dr. Ramsay’s expert identification is complicated by the fact that Plaintiffs did
not cite this evidence in the appropriate disclosure documents. With that said, Dr.
Ramsay stated that the appearance of the subject bears was consistent with that of grizzly
bears in a declaration in support of Plaintiffs’ April 30, 2015, opposition to the Zoo’s
motion for summary judgment. Moreover, the district court—in response to Plaintiffs’
disclosure violation—appears to have given the Zoo an opportunity to designate
additional expert witnesses, an opportunity that the Zoo declined. See Reply Br. at 16.


                                              5
      Finally, Plaintiffs proffered expert testimony that highlighted serious deficiencies

in the Zoo’s treatment of its bears. Dr. Ramsay and Ms. Else Poulson—a zookeeper and

animal behaviorist—testified that the Zoo’s virtually barren concrete pit enclosures,

public feeding arrangements, and apparent lack of meaningful enrichment programs fell

short of generally accepted animal husbandry practices. Ms. Poulsen added that the small

concrete pits prompted the bears to engage in the abnormal behavior of pacing.

Ms. Poulsen, along with Dr. Ramsay, also identified the bears’ act of begging for food as

an abnormal behavior that was attributable to the Zoo’s practice of public feeding and its

inadequate nourishment of the bears.

      The Zoo attempted to push back on Plaintiffs’ evidentiary presentation.

Ms. Coggins testified that the Zoo had described the subject bears as grizzly bears only

for promotional purposes. Additionally, David Ackerman, D.V.M.—the Zoo’s primary

veterinary care provider—testified that the subject bears are European brown bears.

      Ms. Coggins and Dr. Ackerman also testified that the subject bears are in good

health, and do not demonstrate abnormal behavior. Dr. Ackerman added that although

current zookeeping practices for brown bears—a category that includes grizzly bears—

provide for more space and a more natural environment than the Zoo currently provides,

he has had discussions with Mr. Coggins about implementing such practices in the future.

      On March 30, 2016, the district court issued its decision in this case. Hill, 2016

WL 1251190. The court first held that Plaintiffs had standing to litigate their ESA suit,

because Plaintiffs had demonstrated that the Zoo was injuring their aesthetic interest in

viewing the subject bears in a setting compatible with the ESA, in a manner that could be

                                            6
redressed by injunctive relief calling for such a setting. The court then considered the

conflicting evidence, weighed the credibility of witnesses, assessed the relevant discovery

history, and arrived at the conclusion that the subject bears are grizzly bears protected by

the ESA.

       In the end, however, the court ruled against Plaintiffs on the issue of the Zoo’s

ESA liability. After examining the relevant regulations, the court concluded that the

Zoo’s manner of maintaining its bears did not—for ESA purposes—harm or harass the

bears, and by extension did not subject the bears to a taking.

       Of note, the court based its conclusion that the Zoo did not harass its bears entirely

on its determination that the Zoo’s animal husbandry practices complied with applicable

standards under the Animal Welfare Act (AWA), 7 U.S.C. § 2131 et seq. The court

explicitly declined to consider whether the Zoo’s practices complied with “generally

accepted” animal husbandry practices, despite language in the relevant regulation

referencing a “generally accepted” standard. See 50 C.F.R. § 17.3 (explaining that the

definition of “[h]arass” under the ESA excludes “generally accepted . . . [a]nimal

husbandry practices that meet or exceed the minimum standards for facilities and care

under the [AWA]” (emphasis added)). The court also found it unnecessary to consider

whether the Zoo’s practices are of an injurious or disruptive nature.

       After concluding that the Zoo was not liable under the ESA, the court dismissed

with prejudice the entirety of Plaintiffs’ suit. Plaintiffs filed a timely appeal from the

district court’s judgment, and contest the court’s determination that the Zoo is not

committing a taking. The Zoo filed a timely cross-appeal, and contests the court’s

                                             7
determinations that Plaintiffs have standing in this case and that the subject bears are

grizzly bears protected by the ESA. The appeal and the cross-appeal were consolidated,

and we possess jurisdiction to review them both pursuant to 28 U.S.C. § 1291.


                                            II.

       We review a district court’s legal determinations, including its rulings as to

whether a party possesses standing and its interpretations of regulations, de novo. See

Wilson v. Dollar Gen. Corp., 717 F.3d 337, 342 (4th Cir. 2013) (standing); United States

v. Boynton, 63 F.3d 337, 342 (4th Cir. 1995) (interpretation of regulations). We review a

district court’s findings of fact for clear error. See Nelson-Salabes, Inc. v. Morningside

Dev., LLC, 284 F.3d 505, 512 (4th Cir. 2002). “We review a district court’s discovery

rulings, as well as its decision to admit particular expert testimony, for abuse of

discretion.” Bresler v. Wilmington Trust Co., 855 F.3d 178, 189 (4th Cir. 2017).


                                            III.

       As a threshold matter, we must determine whether Plaintiffs possess Article III

standing to bring this suit against the Zoo. See United States v. Under Seal, 853 F.3d

706, 721 (4th Cir. 2017). We conclude that they do.


                                            A.

       To satisfy Article III’s standing requirements, a plaintiff must have “(1) suffered

an injury in fact, (2) that is fairly traceable to the challenged conduct of the defendant,

and (3) that is likely to be redressed by a favorable decision.” Spokeo, Inc. v. Robins, 136


                                             8
S. Ct. 1540, 1547 (2016). “The plaintiff, as the party invoking federal jurisdiction, bears

the burden of establishing these elements.” Id.


                                               B.

         The district court held that Plaintiffs satisfied all three standing elements. We

agree.

         To begin, Plaintiffs’ claim that the Zoo is depriving them of a right to personally

observe the Zoo’s bears living in a setting compatible with the ESA constitutes an

aesthetic injury that satisfies the first standing element of injury in fact.

         “To establish injury in fact, a plaintiff must show that he or she suffered ‘an

invasion of a legally protected interest’ that is ‘concrete and particularized’ and ‘actual or

imminent, not conjectural or hypothetical.’” Spokeo, 136 S. Ct. at 1548 (quoting Lujan v.

Defenders of Wildlife, 504 U.S. 555, 560 (1992)). Courts frequently treat an aesthetic

interest in the observation of animals as a legally protected interest. See Lujan, 504 U.S.

at 562–63 (explaining that “the desire to use or observe an animal species, even for

purely esthetic purposes, is undeniably a cognizable interest for purpose of standing”

(citing Sierra Club v. Morton, 405 U.S. 727, 734 (1972))); Am. Soc’y for Prevention of

Cruelty to Animals v. Ringling Bros. & Barnum & Bailey Circus, 317 F.3d 334, 337

(D.C. Cir. 2003) (concluding that “an injury in fact can be found when a defendant

adversely affects a plaintiff’s enjoyment of flora or fauna, which the plaintiff wishes to

enjoy again upon the cessation of the defendant’s actions”).            When that interest is

invaded in a real, non-speculative, and personal manner, the requirement of an actual or


                                               9
imminent, concrete, and particularized injury is satisfied. See Spokeo, 136 S. Ct. at

1548–49 (explaining the concreteness and particularization conditions); see also Lujan,

504 U.S. at 563–64 (rejecting plaintiffs’ claim that they suffered actual or imminent

injury from government action that allegedly harmed endangered species living in foreign

countries, because the plaintiffs only expressed speculative “‘some day’ intentions” to

visit those countries).

       In this case, Plaintiffs claim a strong interest in observing the Zoo’s bears living in

conditions that do not violate the ESA. They explain, however, that they are precluded

from observing the bears living in such conditions because the bears are currently being

mistreated. Plaintiffs add that they are willing and able to go back and visit the bears if

the conditions that the bears live in are improved. These claims, if true, are sufficient to

establish injury in fact under the relevant precedent.

       Importantly, the district court found Plaintiffs’ claims credible.         The court

defended its finding of injury by highlighting the “spiritual and cultural connection with

the bears” that Plaintiffs, as members of the EBCI, possessed. Hill, 2016 WL 1251190,

at *9. The court also cited definite statements by Plaintiffs confirming their intent to

return to the nearby Zoo if the bears’ setting improved. See, e.g., id. at *3 (noting that

Ms. Walker claimed she “certainly would go” to observe the bears if they were given a

more humane setting); cf. Friends of the Earth, Inc. v. Laidlaw Envt’l Servs. (TOC), Inc.,

528 U.S. 167, 184 (2000) (holding that plaintiffs had standing to sue where they offered

conditional statements that they would use a nearby river if the discharge of pollutants in

the river ceased). The court recognized that Plaintiffs only observed the bears for fifteen

                                             10
to thirty minutes, but reasonably attributed their somewhat short observation time to the

upsetting nature of the bear scene. Hill, 2016 WL 1251190, at *3. We discern no clear

error in these sound credibility determinations.

       Having found that Plaintiffs satisfy the injury in fact element, the second and third

standing elements easily follow. The Zoo is maintaining its bears in the setting that

Plaintiffs complain of, and so Plaintiffs’ alleged aesthetic injury is fairly traceable to the

Zoo. Finally, Plaintiffs claim that they are being deprived of a right to observe the bears

living in a setting that does not violate the ESA, and this can be redressed by an

injunction directing the Zoo to maintain its bears in such a setting.


                                             IV.

                                             A.

       Secure in the justiciability of this case, we now consider whether the bears in this

case are grizzly bears protected by the ESA.          We agree with the district court’s

determination that Plaintiffs have proven that the subject bears are indeed grizzly bears.

       The district court’s determination is corroborated by several pieces of evidence

whose admission is not contested on appeal.             These include the Zoo’s online

representations, signs, and veterinary records—as well as USDA reports—that

collectively identify the subject bears as grizzly bears. Hill, 2016 WL 1251190, at *3–4.

        The district court’s determination is also corroborated by trial testimony from

Plaintiffs’ expert, Dr. Ramsay, who identified the subject bears as grizzly bears based on

his observation of distinctive shoulder humps on the bears. Id. at *5.


                                             11
       The district court’s determination, moreover, was reached after sensibly rejecting

the Zoo’s contrary evidence. The court acknowledged Ms. Coggins’s claim that the

subject bears were referred to as grizzly bears simply for promotional purposes, but found

her testimony in that matter “not credible” in light of the Zoo’s representations to the

USDA that those bears are grizzly bears. Id. The court also acknowledged that the Zoo’s

veterinarian, Dr. Ackerman, had testified that the subject bears are European brown

bears, but concluded that this testimony was undermined by contrary representations in

his veterinary certifications. Id. These are well-reasoned credibility determinations that

we are unwilling to disturb. See F.T.C. v. Ross, 743 F.3d 886, 894 (4th Cir. 2014) (“In

cases in which a district court’s factual findings turn on assessments of witness credibility

or the weighing of conflicting evidence during a bench trial, such findings are entitled to

even greater deference [than usual].” (internal quotation marks omitted)).

       In sum, the district court was entirely justified in concluding that the subject bears

are grizzly bears, and are therefore protected by the ESA.


                                             B.

       Nonetheless, the Zoo contests the district court’s determination that the subject

bears are grizzly bears on the grounds that—in the Zoo’s view—Dr. Ramsay’s expert

identification was improperly admitted.       The basis for the Zoo’s challenge to Dr.

Ramsay’s expert identification is that this evidence was not cited in the disclosure report

produced by Plaintiffs and Dr. Ramsay pursuant to Rule 26 of the Federal Rules of Civil

Procedure. See Fed. R. Civ. P. 26(a)(2)(B)(i) (requiring parties to disclose “complete


                                             12
statement of all opinions the [expert] witness will express and the basis and reasons for

them”). The district court acknowledged this issue, but reasoned that Plaintiffs’ Rule 26

violation was harmless. See Hill, 2016 WL 1251190, at *4 n.6. We affirm.

       “District courts are accorded ‘broad discretion’ in determining whether a party’s

nondisclosure or untimely disclosure of evidence is substantially justified or harmless.”

Bresler, 855 F.3d at 190 (quoting Wilkins v. Montgomery, 751 F.3d 214, 222 (4th Cir.

2014)). In making this determination, a district court should be guided by the five

Southern States factors:

       (1) the surprise to the party against whom the evidence would be offered;
       (2) the ability of that party to cure the surprise; (3) the extent to which
       allowing the evidence would disrupt the trial; (4) the importance of the
       evidence; and (5) the nondisclosing party’s explanation for its failure to
       disclose the evidence.

S. States Rack & Fixture, Inc. v. Sherwin-Williams Co., 318 F.3d 592, 597 (4th Cir.

2003). “The first four factors . . . relate primarily to the harmlessness exception, while

the last factor, addressing the party’s explanation for its nondisclosure, relates mainly to

the substantial justification exception.” Bresler, 855 F.3d at 190. 2

       Regarding the first factor, the Zoo had prior notice of Dr. Ramsay’s opinion that

undermines its claim of unfair surprise. Dr. Ramsay stated that the appearance of the

bears was consistent with that of grizzly bears in a declaration in support of Plaintiffs’


       2
         We recognize that the district court did not explicitly address the Southern States
factors. Even so, “the district court was not required to tick through each of the Southern
States factors. Southern States explains that district courts have ‘broad discretion’ to
decide harmlessness and ‘should’—not ‘shall’—‘be guided by’ the five factors.”
Wilkins, 751 F.3d at 222 (quoting S. States, 318 F.3d at 597).

                                             13
April 30, 2015, opposition to the Zoo’s motion for summary judgment. He provided his

expert identification of the bears at the bench trial almost five months later in late

September 2015.

       As for the second factor, the district court gave the Zoo an opportunity to

designate additional expert witnesses in response to the Zoo’s concerns about timing.

The Zoo therefore had an opportunity to mitigate the effect of any unfair surprise.

Although the Zoo decided not to avail itself of this opportunity, we cannot fault Plaintiffs

for this independent decision made by the Zoo.

       With respect to the third factor, Dr. Ramsay’s expert identification cannot fairly be

labeled a trial disruption. This identification only addressed the discrete point of whether

or not the subject bears are grizzly bears.        It did not “interject an additional, and

considerably complex, legal theory” into the case, nor did it “substantially change the

character of the case and render obsolete much of the parties’ trial preparation.” Rambus,

Inc. v. Infineon Tech. AG, 145 F. Supp. 2d 721, 730 (E.D. Va. 2001).

       Moving on to the fourth factor, Dr. Ramsay’s expert identification was admittedly

important in that it helped establish a prerequisite to Plaintiffs’ claims for relief. The

importance of this identification is somewhat diminished, however, given that Plaintiffs

had already proffered considerable, independent evidence establishing that prerequisite.

       Finally, with regards to the fifth factor, we assume for the sake of argument that

Plaintiffs lacked an adequate explanation for their discovery violation. As noted above,

however, this factor is primarily related to the substantial justification exception, and so it

sheds little light on the harmlessness exception under consideration here.

                                              14
       In sum, the factors most relevant to the harmlessness inquiry weigh in favor of, or

are at least neutral in regards to, the admission of Dr. Ramsay’s expert identification. As

such, the district court did not abuse its broad discretion in excusing Plaintiffs’ non-

compliance with Rule 26 on harmlessness grounds. 3


                                            V.

       We now turn to the heart of this case—the question of whether the district court

correctly held that the Zoo did not engage in an unlawful taking of its captive grizzly

bears. As explained below, we conclude that this holding was the result of incorrect legal

analysis; we consequently vacate this holding and remand this case to the district court

for further consideration.


                                            A.

       The ESA prohibits the “tak[ing]” of any endangered or threatened species, 16

U.S.C. § 1538(a)(1)(B), and makes it unlawful to possess any endangered or threatened

species that has been unlawfully “taken,” id. § 1538(a)(1)(D). Grizzly bears in the lower

forty-eight states are considered threatened species. 50 C.F.R. § 17.11(h).

       3
         The Zoo raises additional challenges to other evidentiary decisions by the district
court, but we decline to address them. The uncontested evidence and Dr. Ramsay’s
expert identification constitute overwhelming evidence that the subject bears are grizzly
bears, such that the Zoo could not possibly have been prejudiced by the arguably
improper admission of any additional evidence confirming that point. See Tire Eng’g &
Distrib., LLC v. Shandong Linglong Rubber Co., Ltd., 682 F.3d 292, 314 (4th Cir. 2012)
(per curiam) (“Rule 61 [of the Federal Rules of Civil Procedure] directs courts to
disregard any error or defect in the proceeding unless the error is prejudicial: It must
have affected the outcome of the district court proceedings.” (internal quotation marks
omitted)).

                                            15
       The ESA expansively defines the term “take” as “to harass, harm, pursue, hunt,

shoot, wound, kill, trap, capture, or collect, or to attempt to engage in any such conduct.”

16 U.S.C. § 1532(19). Plaintiffs contend that the manner in which the Zoo maintains its

bears constitutes harassment and harm proscribed by the ESA. We consider each claim

in turn.


                                            B.

                                             1.

       We begin by addressing Plaintiffs’ harassment claim. The Fish and Wildlife

Service (FWS) of the U.S. Department of the Interior defines “[h]arass” as “an

intentional or negligent act or omission which creates the likelihood of injury to wildlife

by annoying it to such an extent as to significantly disrupt normal behavioral patterns

which include, but are not limited to, breeding, feeding, or sheltering.” 50 C.F.R. § 17.3.

This regulatory definition contains certain exclusions:

       This definition, when applied to captive wildlife, does not include generally
       accepted:

       (1) Animal husbandry practices that meet or exceed the minimum
          standards for facilities and care under the [AWA],

       (2) Breeding procedures, or

       (3) Provisions of veterinary care for confining, tranquilizing, or
          anesthetizing, when such practices, procedures, or provisions are not
          likely to result in injury to the wildlife.

Id. (emphasis added). The Secretary of Agriculture is responsible for promulgating

facilities and care standards under the above-referenced AWA. See 7 U.S.C. § 2143(a);

see also People for the Ethical Treatment of Animals v. United States Dep’t of Agric., 861

                                            16
F.3d 502, 505 n.1 (4th Cir. 2017) (“The [AWA] authorizes the Secretary of Agriculture,

who falls within the USDA, to administer the Act.”).

       At issue in this case is the proper interpretation of the first enumerated exclusion. 4

The district court interpreted this exclusion to excuse animal husbandry practices that are

compliant with applicable AWA standards, without regard to whether those practices are

“generally accepted.” Plaintiffs urge us to reject this interpretation, explaining that the

exclusion can only fairly be interpreted to excuse animal husbandry practices that are

both (1) “generally accepted” and (2) AWA compliant.             We agree with Plaintiffs’

position on this matter.

       Plaintiffs’ interpretation necessarily follows from the relevant regulatory text. The

first enumerated exclusion specifically requires AWA compliance, and it is preceded by a

“generally accepted” requirement that applies to the disjunctive list of enumerated

exclusions. It is therefore clear that the first enumerated exclusion is comprised of both a

“generally accepted” requirement and an AWA compliance requirement.

       The district court’s contrary interpretation renders meaningless the phrase

“generally accepted” in 50 C.F.R. § 17.3. It therefore conflicts with basic principles of

legal interpretation.      See TRW Inc. v. Andrews, 534 U.S. 19, 31 (2001) (“It is

a cardinal principle of statutory [and regulatory] construction that a statute [or regulation]



       4
         Although the Zoo has complained about the clarity of the first enumerated
exclusion, we note that it does not challenge the validity of this exclusion or any other
feature of 50 C.F.R. § 17.3. Thus, this is strictly a case about regulatory interpretation.


                                             17
ought, upon the whole, to be so construed that, if it can be prevented, no clause, sentence,

or word shall be superfluous, void, or insignificant.” (internal quotation marks omitted)). 5

       Moreover, by reading the “generally accepted” requirement out of the first

enumerated exclusion from 50 C.F.R. § 17.3’s definition of harass, the district court

narrows the scope of what constitutes harassment and, by extension, the scope of what

constitutes a proscribed taking of protected animals under the ESA. The district court’s

interpretation also makes it so that the first enumerated exclusion is necessarily satisfied

whenever a defendant complies with the Secretary of Agriculture-administered AWA.

This protection-narrowing, Secretary of Agriculture-centered outcome is in tension with

what the Supreme Court has explained Congress had in mind in enacting the ESA: a

“broad purpose to protect endangered and threatened wildlife,” which was to be advanced

in large part through “broad administrative and interpretive power [delegated] to the

Secretary [of the Interior].” Babbitt v. Sweet Home Chapter of Cmtys. for a Great

Oregon, 515 U.S. 687, 700, 708 (1995) (citing 16 U.S.C. §§ 1533, 1540(f)).

       The impropriety of treating as meaningless the “generally accepted” language in

50 C.F.R. § 17.3 is especially apparent when one considers the entire set of exclusions

impacted by that language. Specifically, the second enumerated exclusion from 50

C.F.R. § 17.3’s definition of harass excuses “generally accepted . . . [b]reeding

procedures.” If the phrase “generally accepted” was deemed meaningless, then we would


       5
         “We normally construe regulations using the same rules we employ to construe
statutes.” Harris v. Norfolk S. Ry. Co., 784 F.3d 954, 962 (4th Cir. 2015).


                                             18
end up with the absurd result whereby all breeding procedures—from the benign to the

cruel—would fall outside the scope of the regulatory definition of harass. This cannot be

so. See Chesapeake Ranch Water Co. v. Bd. of Comm’rs of Calvert Cty., 401 F.3d 274,

280 (4th Cir. 2005) (cautioning against interpretations of text that lead to “an absurd

conclusion”) (quoting In re Chapman, 166 U.S. 661, 667 (1897)).


                                             2.

       Having rejected the district court’s interpretation of the first enumerated exclusion

from 50 C.F.R. § 17.3’s definition of harass, we now address the appropriate disposition

for this case.

       To establish harassment in this case, Plaintiffs must prove (1) that the Zoo’s

animal husbandry practices fall within 50 C.F.R. § 17.3’s definition of harass, and

(2) that those practices do not fall within the first enumerated exclusion from that

definition. The first issue remains unresolved because the district court did not reach it.

The second issue remains unresolved in light of our holding that the district court

improperly declined to ask whether the Zoo’s animal husbandry practices are “generally

accepted” before it invoked the first enumerated exclusion. 6

       It is therefore appropriate to remand this case to the district court to resolve these

issues in the order of its choosing. See Singleton v. Wulff, 428 U.S. 106, 120 (1976) (“It


       6
          As for the district court’s finding that the Zoo’s animal husbandry practices
satisfy the AWA compliance requirement of the first enumerated exclusion, we accept
that finding as true, because Plaintiffs have not contested it on appeal.


                                             19
is the general rule, of course, that a federal appellate court does not consider an issue not

passed upon below.”). We add that if the district court rules against Plaintiffs on one of

these issues, then it need not reach the other issue, because Plaintiffs must prevail on both

issues in order to establish ESA liability.


                                              C.

       In addition to challenging the district court’s rejection of its claim that the Zoo

engaged in a taking by harassing the grizzly bears, Plaintiffs also briefly challenge the

court’s rejection of its claim that the Zoo engaged in a taking by harming the grizzly

bears. We reserve judgment on this challenge.

       We do so as a result of the unique posture of this case.           To elaborate, the

regulatory definition of harass contains requirements that are less demanding for

Plaintiffs—whose suit centers on behavioral interference evidence—than are the

requirements contained in the regulatory definition of harm. 7 Therefore, we believe it is

prudent to grant the district court an opportunity to address the application of the

regulatory definition of harass in the first instance before we review the difficult question

of the application of the regulatory definition of harm. This course of action is especially

appropriate in light of the fact that the parties’ appellate briefs focused primarily on

       7
         Compare 50 C.F.R. § 17.3 (defining “[h]arass” as “an intentional or negligent act
or omission which creates the likelihood of injury to wildlife by annoying it to such an
extent as to significantly disrupt normal behavioral patterns which include, but are not
limited to, breeding, feeding, or sheltering”) with id. (defining “[h]arm” as “an act which
actually kills or injures wildlife. Such act may include significant habitat modification or
degradation where it actually kills or injures wildlife by significantly impairing essential
behavioral patterns, including breeding, feeding or sheltering”).

                                              20
analyzing harassment, not harm. Cf. Goldfarb v. Mayor & City Council of Baltimore,

791 F.3d 500, 515 (4th Cir. 2015) (reserving judgment on a question outside of what the

“appellate briefs centered on,” in a case that was being remanded to the district court).


                                             VI.

       For the foregoing reasons, we affirm the district court’s determinations that

Plaintiffs have standing in this case and that the subject bears are grizzly bears.

       We conclude, however, that the district court’s determination that the Zoo is not

committing a taking was based on incorrect legal analysis. We therefore vacate that

determination and remand this case for further proceedings consistent with this opinion.

                                                                 AFFIRMED IN PART;
                                                    VACATED IN PART AND REMANDED




                                             21
BAILEY, District Judge, concurring in part and dissenting in part:

       I am pleased to concur in that part of the majority opinion affirming the District

Court’s decision with respect to Article III standing and the fact that the subject bears are

indeed grizzly bears.     I feel compelled, however, to respectfully dissent from the

majority’s interpretation of 50 C.F.R. § 17.3.

       50 C.F.R. § 17.3 provides:

       Harass in the definition of "take" in the Act means an intentional or

       negligent act or omission which creates the likelihood of injury to wildlife

       by annoying it to such an extent as to significantly disrupt normal

       behavioral patterns which include, but are not limited to, breeding, feeding,

       or sheltering. This definition, when applied to captive wildlife, does not

       include generally accepted:

              (1)   Animal husbandry practices that meet or exceed the

              minimum standards for facilities and care under the Animal

              Welfare Act,

              (2) Breeding procedures, or

              (3) Provisions of veterinary care for confining, tranquilizing,

              or anesthetizing, when such practices, procedures, or

              provisions are not likely to result in injury to the wildlife.

       Harm in the definition of "take" in the Act means an act which actually kills

       or injures wildlife. Such act may include significant habitat modification or

       degradation where it actually kills or injures wildlife by significantly

                                              22
       impairing essential behavioral patterns, including breeding, feeding or

       sheltering.

50 C.F.R. § 17.3.

       “‘When a species ... is listed as either “threatened” or “endangered” under the

[ESA], it is then subject to a host of protective measures designed to conserve the

species.’ Safari Club Int'l v. Salazar (In re Polar Bear Endangered Species Act Listing &

Section 4(d) Rule Litig. - MDL No. 1993), 709 F.3d 1, 2 (D.C. Cir. 2013). The species

are subject, for example, to the section 9 prohibitions, which make it unlawful ‘for any

person subject to the jurisdiction of the United States’ to, inter alia, ‘import[,]’ ‘export

[,]’ ‘possess, sell, deliver, carry, transport, or ship, by any means whatsoever[,]’ ‘take any

such species within the United States or the territorial sea of the United States[,]’ ‘deliver,

receive, carry, transport, or ship in interstate or foreign commerce, by any means

whatsoever and in the course of a commercial activity, any such species[,]’ or to ‘sell or

offer for sale in interstate or foreign commerce any such species[.]’ 16 U.S.C. § 1538(a);

see also Humane Soc'y of U.S. v. Kempthorne, 527 F.3d 181, 182 (D.C. Cir. 2008); . . ..

       “The prohibition on ‘take’ means that it is unlawful ‘to harass, harm, pursue, hunt,

shoot, wound, kill, trap, capture, or collect, or to attempt to engage in any such conduct.’

16 U.S.C. § 1532(19). In particular, the term ‘harm’ refers to ‘an act which actually kills

or injures wildlife[,]’ while the term ‘harass’ means ‘an intentional or negligent act or

omission which creates the likelihood of injury to wildlife by annoying it to such an

extent as to significantly disrupt normal behavioral patterns which include, but are not

limited to, breeding, feeding or sheltering.’ 50 C.F.R. § 17.3. When applied to captive

                                              23
animals, the definition for ‘harass’ does not include the ‘generally accepted’ practices of

animal husbandry, breeding, or aspects of veterinary care. Id.” Safari Club Int'l v.

Jewell, 960 F. Supp. 2d 17, 30-31 (D. D.C. 2013).

       For a threatened species, like the grizzly bear, the ESA provides that the FWS or

the National Marine Fisheries Service shall promulgate regulations that they deem

“necessary and advisable to provide for the conservation of such species,” including

applying some or all of the Section 9 prohibitions to the threatened species. 16 U.S.C. §

1533(d).

       FWS regulations specifically prohibit the “taking” of any grizzly bear in the 48

conterminous states of the United States, including North Carolina. 50 C.F.R. §

17.40(b)(1)(i)(A).

       In promulgating the exception for captive animals contained in 50 C.F.R. § 17.3,

the Fish and Wildlife Service stated that the “purpose of amending the Service's

definition of ‘harass’ is to exclude proper animal husbandry practices that are not likely

to result in injury from the prohibition against ‘take.’ Since captive animals can be

subjected to improper husbandry as well as to harm and other taking activities, the

Service considers it prudent to maintain such protections, consistent with Congressional

intent.” Captive-bred Wildlife Regulation, 63 FR 48634-02 (September 11, 1998).

       The FWS further stated that “‘Harass’ under the definition of ‘take’ in §17.3 is an

act or omission that creates the likelihood of injury by annoying wildlife to such an extent

as to significantly disrupt normal behavior patterns. The applicability of this concept to

captive-held animals has been unclear, since human activities, including normal

                                            24
husbandry practices, provided in caring for captive-held wildlife in all probability disrupt

behavior patterns.” Id.

       The FWS added that “[i]n light of this, the definition of ‘harass’ in 50 CFR 17.3 is

modified to exclude normal animal husbandry practices that are not likely to result in

injury such as humane and healthful care when applied to captive wildlife. While no

permit is required to possess lawfully acquired listed wildlife, a person cannot possess

wildlife without doing something to it that might be construed as harassment under a

literal interpretation of the definition in use since 1979, e.g., keep it in confinement,

provide veterinary care, etc. Under this scenario, a person who legally possessed wildlife

without a permit could be considered in violation of the prohibition against harassment

unless they obtained a specific permit that authorized them to conduct normal animal

husbandry activities. Had Congress intended this result, the prohibition on possession in

section 9 of the Act would not have been limited to endangered species taken in violation

of the Act.” Id.

       The crux of this case is the appropriate construction of 50 C.F.R. § 17.3. An issue

of statutory construction is reviewed de novo. United States v. Hilton, 701 F.3d 959 (4th

Cir. 2012).

       The interpretation adopted by the majority would have the standards to be applied

to holders of captive, threatened animals established, not by the FWS, but rather by some

amorphous set of "generally applicable" standards adopted by the AZA (representing less

than 10% of the zoos in this country) or some other group.     In analyzing the regulation,

it is important to recall that the statute provides criminal sanctions for violations of its

                                            25
terms or of the regulations adopted pursuant thereto - a fact the majority ignores. In

short, the ESA has both criminal and non-criminal aspects.

      In light of the criminal aspect, the rule of lenity could be deemed to be in play. “It

is a basic principle of due process that an enactment is void for vagueness if its

prohibitions are not clearly defined. Vague laws offend several important values. First,

because we assume that man is free to steer between lawful and unlawful conduct, we

insist that laws give the person of ordinary intelligence a reasonable opportunity to know

what is prohibited, so that he may act accordingly. Vague laws may trap the innocent by

not providing fair warning. Second, if arbitrary and discriminatory enforcement is to be

prevented, laws must provide explicit standards for those who apply them. A vague law

impermissibly delegates basic policy matters to policemen, judges, and juries for

resolution on an ad hoc and subjective basis, with the attendant dangers of arbitrary and

discriminatory application.” Grayned v. City of Rockford, 408 U.S. 104, 108-09 (1972)

(footnotes omitted).

      The rule of lenity “reflects not merely a convenient maxim of statutory

construction. Rather, it is rooted in fundamental principles of due process which mandate

that no individual be forced to speculate, at peril of indictment, whether his conduct is

prohibited. Grayned v. City of Rockford, 408 U.S. 104, 108 (1972); United States v.

Harriss, 347 U.S. 612, 617 (1954); Lanzetta v. New Jersey, 306 U.S. 451, 453 (1939);

McBoyle v. United States, 283 U.S. 25, 27 (1931). Thus, to ensure that a legislature

speaks with special clarity when marking the boundaries of criminal conduct, courts must

decline to impose punishment for actions that are not ‘plainly and unmistakably’

                                            26
proscribed. United States v. Gradwell, 243 U.S. 476, 485, 37 S.Ct. 407, 410, 61 L.Ed.

857 (1917).” Dunn v. United States, 442 U.S. 100, 112-13 (1979).

       “The rule of lenity is based on two substantial considerations. First, the rule

recognizes that ‘a fair warning should be given to the world in language that the common

world will understand, of what the law intends to do if a certain line is passed.’ Yi v. Fed.

Bureau of Prisons, 412 F.3d 526, 535 (4th Cir. 2005) (quoting Babbitt v. Sweet Home

Chapter of Cmtys., 515 U.S. 687, 704 n. 18 (1995)). Second, the rule acknowledges that

Congress, rather than the judiciary, is the proper institution to define criminal conduct.

Id.” United States v. Hilton, 701 F.3d 959, 968 (4th Cir. 2012).

       While it is unclear whether the rule of lenity applies in a civil dispute, in Esquivel-

Quintana v. Lynch, 810 F.3d 1019 (6th Cir. 2016), reversed, 137 S.Ct. 1562 (2016), the

Sixth Circuit noted that the reasons for the rule are equally applicable in cases where a

regulation has both civil and criminal ramifications, stating that “[a]n increasingly

emergent view asserts that the rule of lenity ought to apply in civil cases involving

statutes that have both civil and criminal applications. See Whitman v. United States, ___

U.S. ___, 135 S.Ct. 352, 352-54 (2014) (Scalia, J., statement respecting denial of

certiorari); Carter v. Welles-Bowen Realty, Inc., 736 F.3d 722, 729-36 (6th Cir. 2013)

(Sutton, J., concurring). This view is based on two principles. First, statutory terms

should not have different meanings in different cases - ‘a statute is not a chameleon.’

Carter, 736 F.3d at 730. Second, ambiguous statutes must be construed in favor of

defendants under the rule of lenity.      The rule of lenity ensures that the public has

adequate notice of what conduct is criminalized, and preserves the separation of powers

                                             27
by ensuring that legislatures, not executive officers, define crimes. Taken together, these

two principles lead to the conclusion that the rule of lenity should apply in civil cases

involving ambiguous statutes with criminal applications.” Esquivel-Quintana, at 1023.

         The Supreme Court has suggested that the rule of lenity should apply in such

cases.    In Leocal v. Ashcroft, 543 U.S. 1 (2004), the Court reviewed a Board of

Immigration Appeals decision interpreting 8 U.S.C. § 1101(a)(43)(F). 543 U.S. 1, 8-13

(2004). That provision states that a conviction for a ‘crime of violence (as defined in

section 16 of Title 18, but not including a purely political offense)’ counts as an

aggravated felony if it is punishable by at least one year of imprisonment. The Court held

that ‘crime of violence’ did not include the petitioner's Florida DUI conviction, and

added in a footnote:

         Even if § 16 lacked clarity on this point, we would be constrained to

         interpret any ambiguity in the statute in petitioner's favor. Although here

         we deal with § 16 in the deportation context, § 16 is a criminal statute, and

         it has both criminal and noncriminal applications.          Because we must

         interpret the statute consistently, whether we encounter its application in a

         criminal or noncriminal context, the rule of lenity applies. Cf. United

         States v. Thompson/Center Arms Co., 504 U.S. 505, 517–518 (1992)

         (plurality opinion) (applying the rule of lenity to a tax statute, in a civil

         setting, because the statute had criminal applications and thus had to be

         interpreted consistently with its criminal applications).

543 U.S. at 12, n. 8.

                                               28
       Similarly, in Kasten v. Saint-Gobain Performance Plastics Corp., 563 U.S. 1

(2011), and Maracich v. Spears, ___ U.S. ___, 133 S.Ct. 2191, 2209 (2013), the Court

suggested that the rule of lenity could apply if an ambiguity existed, but had no occasion

to apply it because the statute was unambiguous.” Id.

       An application of the rule of lenity to the regulatory framework adopted by the

majority clearly indicates that the same cannot pass muster.             As envisioned by the

majority, whether an action or inaction on the part of a zookeeper was legal would

depend on the current opinion, not codified in any form, of non-government members of

certain associations or the general public. Such a framework hardly provides a person

with fair warning of what the law intends to do if a certain line is passed. In addition,

such a framework violates the separation of powers by allowing non-governmental

entities, not legislatures, or even executive officers, define crimes.

       Inasmuch as the majority’s framework is unworkable and violative of due process,

the only appropriate reading of the regulation is that the Secretary of Agriculture, taking

into consideration generally accepted practices, is to determine, establish, and enforce the

minimum standards for operators holding captive, threatened animals.

       Were the rule of lenity not to apply, the majority’s interpretation of the regulation

still violates the rubrics of statutory construction.

       In interpreting a statute, “[w]e give the words of a statute their ordinary,

contemporary, common meaning, absent an indication Congress intended them to bear

some different import.” Wall v. Kholi, 562 U.S. 545, 551 (2011), quoting Williams v.

Taylor, 529 U.S. 420, 431 (2000).

                                               29
       “It is ‘a cardinal principle of statutory construction’ that ‘a statute ought, upon the

whole, to be so construed that, if it can be prevented, no clause, sentence, or word shall

be superfluous, void, or insignificant.’ Duncan v. Walker, 533 U.S. 167, 174 (2001)

(internal quotation marks omitted); see United States v. Menasche, 348 U.S. 528, 538-39

(1955) (‘It is our duty “to give effect, if possible, to every clause and word of a statute.”’

(quoting Montclair v. Ramsdell, 107 U.S. 147, 152 (1883))).” TRW Inc. v. Andrews, 534

U.S. 19, 31 (2001).

       The District Court was correct in its conclusion of law that according to the plain

language of 50 C.F.R. § 17.3, an exhibitor’s husbandry practices which comply with the

minimum standards for facilities and care under the AWA fall outside the definition of

“harassment” as set forth in the ESA and in concluding that “[o]nly when the exhibitor's

practices fail to meet the minimum standards established by the Animal Welfare Act can

such practices constitute ‘harassment’ of a captive endangered or threatened species.”

Hill v. Coggins, 2016 WL 1251190, at *13 (W.D. N.C. Mar. 30, 2016).

       The focus of 50 C.F.R. § 17.3(1) is on the standards promulgated under the AWA

- not upon some ambiguous and undefinable “generally accepted” standards disconnected

from the standards of the AWA. Adopting the majority’s interpretation ignores the clear

intent of the ESA to allow the AWA to establish the standards regarding acceptable

husbandry practices. Under 16 U.S.C. § 1533(d), it is the FWS that is to promulgate

regulations that are deemed “necessary and advisable to provide for the conservation of

such species.”



                                             30
       The majority’s interpretation also places the court in the untenable position of

being required to become a non-judicial rule making body determining exactly what are

“generally accepted” animal husbandry practices. Are the accreditation standards of the

AZA, a voluntary organization that encompasses less than ten percent of the exhibitors in

the United States necessarily “generally accepted?” The difficulty in determining what is

a “generally accepted” husbandry practice is proof that the issue is not one for judicial

determination. Rather, the determination of what is “generally accepted” is why the ESA

defers to the AWA on this issue.

       The District Court’s interpretation of 50 C.F.R. § 17.3 does not permit the AWA

standards to supercede the ESA’s authority to protect threatened species. Rather, the

regulation utilizes the framework of the AWA for evaluation of the adequacy of animal

husbandry practices for captive animals. Should the FWS become unsatisfied with the

standards of the AWA, the FWS has the authority to amend the regulatory scheme to

provide for more stringent protections for threatened or endangered species.

       The Plaintiffs’ argument that the FWS regulatory language creating the “harass”

exception for captive wildlife found at 63 Fed. Reg. 48636, requires that the courts look

outside the enforcement of the AWA by the Department of Agriculture’s Animal Plant

and Health Inspection Service (“APHIS”) to determine what is “generally acceptable” 1 is



1
  “FWS made it clear that in determining whether treatment of captive endangered species was
considered ‘generally accepted’ under the captive wildlife exception to ‘harass’ it was not
looking only to [APHIS], which is charged with administering the AWA, but also to
‘knowledgeable persons in the zoo and aquarium communities.’” Brief of Appellants at 29-30.


                                            31
not a proper interpretation of that provision. A full reading of the surrounding language

with the comments section supports the opposite conclusion - that the Fish and Wildlife

Service decides the applicable standards for animal husbandry:

      To evaluate facilities and care provided by applicants, the [Fish and

      Wildlife Service] will continue to consult with experts such as the

      Department of Agriculture’s Animal and Plant Health Inspection Service,

      which is charged with administering the Animal Welfare Act, and

      knowledgeable persons in the zoo and aquarium communities and the

      private sector as needed.

Id.

      Rather than allowing for private experts to testify what the appropriate standards

for animal husbandry are, this language indicates that the FWS may consult with experts

at APHIS and private experts in determining whether any change in the standards is

warranted.   This comment in no way makes private expert opinions that were not

incorporated by the FWS into the ESA relevant to the issue as to the applicable standard

of “generally accepted animal husbandry practices that meet or exceed the minimum

standard for facilities and care under the Animal Welfare Act.” 50 C.F.R. § 17.3(1). As

a result, the District Court did not err in its conclusion that “[w]hether the CBZ's

practices are generally accepted by other zookeepers or meet certain standards

established by state law or voluntary accrediting associations such as the AZA is not

relevant.” 2016 WL 1251190, at *13.



                                           32
       The majority expresses concern that the District Court’s construction of § 17.3

would negate the breeding procedure and veterinary care portions of the regulation. It is

readily apparent that the drafters of the regulation saw fit to treat animal husbandry

differently than the other provisions.

       There is a rational explanation for this differential. The standard of care for

veterinary practice is, like the standard of care or medical practice, well established.

Breeding practices are virtually a subset of the veterinary standard. Animal husbandry

practices are not so well established and, as noted, above, should not be left to an

amorphous segment of expert or public opinion.

       The only appropriate reading of the regulation is that the Secretary of Agriculture,

taking into consideration generally accepted practices, is to determine, establish, and

enforce the minimum standards for operators holding captive, threatened animals.

                                         I would affirm the judgment of the District Court.




                                            33
