0051105

COMMENTARY

Disturbance,Habituation, and Managementof WaterbirdColonies

IANC. T. NISBET

I.C.T. Nisbet & Company, 150 Alder Lane, North Falmouth, MA 02556, USA Internet: [email protected]

Abstract.-This Commentary presents a critique of studies of effects of human disturbance on breeding colonial waterbirds, including a recent review by Carney and Sydeman (1999). It challenges the mind-set that the effects of disturbance are always adverse, and the resulting management principle that disturbance should be minimized. I argue that many studies do not withstand critical scientific scrutiny, and that published papers and reviews system- atically overstate the adverse effects of human disturbance. I propose definitions of the terms "disturbance", "habit- uation" and "tolerance", as well as classifications of types of disturbance and types of effect. Contrary to prevailing opinions, there is little scientifically acceptable evidence that human disturbance causes substantial harm to terns (Sternaspp.), gulls (Larus spp.) or herons (Ardeidae), although it is likely that sporadic incidents of harassment and vandalism are under-reported. Convincing evidence of adverse effects has been presented for several other species and groups of species; most well-documented cases have been early in the nesting cycle and/or mediated by diurnal avian predators. Although there are no formal studies of habituation, many or most colonial waterbirds can become extremely tolerant of repeated human disturbance. I recommend that, where appropriate, waterbird colonies should be managed for multiple uses (including research, education, and recreation) by deliberately promoting habituation. Although many field biologists are careful to investigate the effects of their activities and are successful in minimizing them, others appear insufficiently aware of the potential for harm, so that there is a need for more complete guidelines and better training. Key words.-Behavior, breeding, colony, disturbance, habituation, investigator, management, terns, tolerance, visitor, waterbirds. Waterbirds 23(2): 312-332, 2000

This journal (formerly Colonial Water- valued. I believe that waterbird colonies are birds) has published more papers on the ef- important resources for scientific research, fects of human disturbance on colonial education, and recreation, but that these waterbirds than any otherjournal, including resources are under-used because the scien- a symposium (Rodgers and Burger 1981) tific community repeatedly overstates the ad- and several reviews. This Commentary ar- verse effects of human disturbance, so that gues that many findings reported in the liter- managers unnecessarily restrict the activities ature and cited by reviewers do not of investigators and visitors. withstand critical scientific scrutiny. Many This Commentary has been stimulated studies did not show adverse effects, or by the review by Carney and Sydeman (1999) showed effects only in special circumstances and includes a critique of that paper. How- that are easily avoided; many other studies ever, my comments on that paper and the were poorly controlled, poorly reported, or studies cited therein are intended to apply otherwise inconclusive. I believe that the also to other reviews and other studies. I pre- basic concepts and terms are ill-defined, and cede this critique with a discussion of term- that the scientific questions and manage- inology, definitions, and classification of ment issues have been poorly framed. I be- effects. I continue with my own summary lieve that important effects are under- of the available information on effects of dis- reported, but that the published studies and turbance on terns, the species with which I reviews are biased and overstate the signi- am most familiar. I discuss briefly the litera- ficance of human disturbance, especially ture on other colonial waterbirds, and con- investigator activity. I believe that the impor- clude with a discussion of management tant phenomena of tolerance and habitua- implications and recommendations for man- tion have been under-reported and under- agement and further research.

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My comments and conclusions are limit- magnitude of the effects, and whether they ed to the geographical areas where most of are significantly adverse. the published studies have been conducted: 3. The proposed definition includes all North America, Europe, Australia, and Ant- forms of activity, including deliberate perse- arctica. It is likely that human persecution cution and vandalism, as well as activities and disturbance of colonial waterbirds are such as casual intrusions that are not direct- more pervasively harmful in other areas ed at the birds in any way. Hence, it is neces- (e.g., Gonzailez 1999), but there is little pub- sary to classify and describe the activities lished information to support conclusions or before meaningful conclusions can be generalizations. drawn about effects of "disturbance". 4. The proposed definition is intended to TERMINOLOGY,DEFINITIONS, exclude habitat modification (e.g., removing AND CLASSIFICATIONOF EFFECTS nest-trees or erecting buildings on an is- land), which makes sites that were previously Disturbance occupied by colonial waterbirds unsuitable or unavailable. Although the act of modify- So far as I can determine, the term "dis- ing the habitat may disturb birds at the time turbance" has not been defined in any of the it is carried out, I distinguish this immediate prior reviews. Within the context of effects effect of disturbance from the permanent ef- on colonial waterbirds, I propose the follow- fect of human development or other forms ing definition: of habitat modification. This distinction is obscured in many previous discussions of the Human disturbance is any human activity subject. that changes the contemporaneous behavior or physiology of one or more individuals within a breeding Types of Disturbance colony of waterbirds. Most previous reviews (e.g., Carney and This definition has four important fea- Sydeman 1999) have made a binary distinc- tures: tion between "investigator disturbance" and 1. "Disturbance"is defined as human ac- "visitordisturbance", but this classification is tivity, not as the response of birds to this ac- insufficient because both classes include tivity. In the literature on colonial widely varying activities, and investigators waterbirds, the term is usually used in the perform many of the same actions as non-in- former sense, but is sometimes used in the vestigators. I propose the following classifica- latter sense. For example, the caption to Fig. tion of human activities, recognizing that 3 in Anderson and Keith (1980) includes the finer subdivisions may be required to ad- phrase "Disturbance can be seen every- dress some management questions: where", referring to birds flying in response 1. "Research procedures" are defined as to human intrusion. In that and other pa- activities by investigators that are applied to pers, the term is used in both senses, or am- individual birds or nests (e.g., marking nests, biguously. For clarity and precision, I trapping, banding, taking blood, applying recommend that it should be used only in radio transmitters). The focus of studies of the sense proposed here, i.e., as the human these procedures is determining the toler- activity that disturbs birds. ance of individual birds or pairs and, if nec- 2. Under the proposed definition, "dis- essary, modifying the procedures to reduce turbance" always results in some effect on or eliminate adverse effects. the birds. In my opinion, it makes no sense 2. "Investigatorintrusions" are defined as to call activity "disturbance" if the birds do activities by investigators (e.g, counting not respond in any way.Hence, it is meaning- nests, banding chicks, walking through the less to ask whether disturbance causes ef- nesting area to enter blinds, etc.) that affect fects: the important issues are the nature and birds other than those individually targeted. 0051107

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The focus of studies of these activitiesis de- help to interpret information on effects of termining the effects of intrusions on the other types of disturbance and harassment. colony as a whole (e.g., the extent to which 8. "Persecution, harassment, and vandal- entering the colony repeatedlyand conduct- ism" is defined as activity by persons (other ing researchmakes birds other than those di- than managers) intended to harm the birds rectly targeted neglect or abandon their (e.g., taking eggs, destroying nests or nest- nests, or facilitatespredation). trees, or pursuing birds in vehicles). 3. "Visitorintrusions" are defined as ac- tivities visitors than by (other investigators) Types of Effect within a waterbirdcolony. These can be sub- classified into "deliberateintrusions" (e.g., Different types of effect that have been by people who enter the nesting area specif- reported in the literature are listed here in ically to see or photograph the birds) and approximate order of increasing severity: "casualintrusions" (e.g., by people who en- 1. Physiological effects (e.g., increases in ter the nesting areafor recreationalor other heart rate) without overt changes in behav- purposes); the latter activities are usually ior. These effects, where demonstrable, show more varied and more difficult to control. that the birds are aware of the human activity "Deliberate intrusions" include cases in and may be "stressed" by it, but should not whichwaterbirds establish colonies withinar- be classified as "adverse" unless it can be eas of human activity(e.g., when herons set- shown that they result in reductions in sur- tle and breed in urbanareas, or gulls or terns vival or reproductive success. nest on buildings). The focus of studies of 2. Walking or flying off the nest, returning these activitiesis usuallyto determine what after the disturbance ends. Again, these ef- activitiesare tolerated by the birds and the fects should not be regarded as "adverse"un- extent to which visitation needs to be re- less the absence from the nest is sufficiently stricted,guided, or controlled. prolonged to result in losses of eggs or chicks 4. "Visitorapproaches" are defined as ac- (e.g., from chilling, overheating, or preda- tivitiesby visitorsthat do not involvepenetra- tion), or the metabolic costs to the parents tion into the nesting area (e.g., using a beach are sufficient to cause nest desertion or re- adjoining a waterbirdcolony). The focus of duced survival. This type of effect includes studiesof these activitiesis usuallydetermin- displacement of loafing, non-breeding, or ing "approachdistances": distances from the prospecting birds from the colony-site; in this edge of the nesting areawithin which visitor case, the effects should not be regarded as approaches start to induce measurable re- "adverse"unless the disturbed birds fail to re- sponses. turn to the site or do not settle to breed there. 5. "Vehicle activities" are defined as 3. Desertion of the nest by one or both movements of motor vehicles, boats, or air- members of a pair. Although potentially an craftthrough, near, or over bird colonies. adverse effect, this does not necessarily re- 6. "Positivemanagement" is defined as sult in a reduction in breeding success, be- activityby managersdesigned to benefit the cause many pairs re-lay after desertion. birds (e.g., posting, wardening,and/or en- 4. Abandonment of the colony-site by tering the colony to control predators).This some or all pairs (including failure of some often involvessome intrusion into the nest- pairs to settle at the site). Although this is usu- ing areas and consequent disturbance. ally classifiable as an adverse effect, the conse- 7. "Negative management" is defined as quences may not be major if the birds relocate activity by managers designed to reduce and breed successfully at another site. Pro- numbers or activity of birds (e.g., harassing longed or permanent reduction in the num- or killing birds, or modifying the habitat). bers nesting at a site should normally be Although this is not usually included within regarded as an adverse effect, because alterna- the term "disturbance", documentation of tive sites will often be less favorable (if not, they the effects of negative management may would have been occupied in the first place). 0051108

DISTURBANCE,HABITUATION AND MANAGEMENT 315

5. Reduction in hatching success, or or "[S]timulus-specific waning of response; deaths of individual chicks. Although usually learning not to respond to something on classifiable as adverse effects, the conse- finding that nothing significant is contin- quences may not be significant if there is gent upon its occurrence" (Immelmann and compensatory survival of other chicks within Beer 1989). Rigorous documentation of ha- the brood. bituation requires longitudinal measure- 6. Reduction in breeding success. This ments of response in individuals subject to usually requires measurement of productivi- controlled repetition of the same stimulus. ty of individual pairs and statistical docu- This has rarely been attempted with colonial mentation of reduction in productivity, waterbirds (but see Wfirm and Hfippop either of experimental groups or the entire 1998). Although habituation to human dis- colony. Either requires rigorous comparison turbance has often been reported in colonial with appropriate reference groups or colo- waterbirds, what is actually described is vari- nies. ation in tolerance. I define "tolerance" as 7. Deaths of individual adults, resulting "the intensity of disturbance that an individ- either from research procedures or from ual bird tolerates without responding in a de- predation that is facilitated by the distur- fined way."Tolerance is easily measured and bance. may vary among individuals or groups of in- 8. Reduction in local, regional, or total dividuals for reasons other than prior expe- populations. rience of disturbance. Demonstrating that For the reasons stated, I believe that ef- tolerance is higher in disturbed colonies fects (1-2) should not be classified as ad- than in undisturbed colonies, or is higher in verse, and effects (3-5) should not be colonies that have been disturbed for longer classified as adverse without either qualifica- periods, provides strong suggestive evidence tion or presentation of evidence for adverse for habituation, but proof of habituation re- consequences on numbers or productivity. quires sequential measurements of toler- Only effects (6-8) should be classified defini- ance within the same individuals or groups. tively as adverse. For this reason, I use only the term tolerance except in the context of management. Documentation of Cause-Effect

Relationships CRITIQUE OF THE PAPER BY CARNEY Much of the literature purporting to show AND SYDEMAN adverse effects of human disturbance-espe- Carney and Sydeman (1999; hereafter, cially effects of uncontrolled activities by C&S) summarized 64 articles that had re- non-investigators-is anecdotal at best. An- ported studies of effects of human distur- ecdotes and correlations are useful in gener- bance on nesting colonial waterbirds.Without ating hypotheses, but they do not provide conducting an intensive search, I quickly strong evidence for causal relationships. In found 64 more and on the my opinion, the same scientific standards papers reports subject, including a handbook article (Nis- should be applied to inferring cause-effect bet 1977) and three reviews (G6tmark 1992; relationships between disturbance and ad- Burger and Gochfeld 1994; Nimon and verse effects as to inferring causal relation- Stonehouse 1995). However C&S selected ships with other environmental factors (e.g., papers for review, their paper appears to predation, food availability,or weather). have been directed primarily towards cata- Habituation and Tolerance loguing adverse effects of disturbance and it often mis-cited, selectively cited, or overstat- Habituation is defined as "the relatively ed such effects. For example, the text of the persistent waning of a response as a result of paper cited 32 papers as having reported repeated stimulation which is not followed that human disturbance reduced produc- by any kind of reinforcement" (Hinde 1970) tivity, breeding success, or reproductive suc- 0051109

316 WATERBIRDS cess in one or more species. In fact, about HUMAN DISTURBANCE IN TERN COLONIES one-third of these papers did not report such effects, and in at least one other the distur- Most of this commentary will be ad- dressed to the of with bance was so poorly documented that its ef- terns, group species I the most fect would not have been accepted by critical which have experience. reviewers (Table 1). In several other cases, the effects cited were associated only with Research Procedures the most intrusive research techniques and did not occur when less intrusive studies One of my own papers (Nisbet 1981) was were carried out. In still other cases, effects repeatedly mis-cited by C&S. Nisbet (1981) were reported only in colonies in which the did not report that investigator disturbance birds were not habituated to human activi- lowered reproductive success of terns (as ties, and did not occur in habituated colo- stated by C&S on p. 71). My study investi- nies. Although habituation was mentioned gated behavioral responses to trapping by C&S several times in the text and once in adults at the nest (as stated in their Table 1). their Table 2 (both in relation to investigator I reported that behavioral responses by Com- disturbance), it was not mentioned in their mon Terns (Sterna hirundo) were minimal. I section on visitor disturbance, in their Table reported that three pairs of Roseate Terns 3, in their recommendations for research, in (Sterna dougallii) had deserted their nests their Abstract, or in their Key Words. Be- when trapped early in incubation in a pilot cause their review thus was focused on stud- study in 1970. However, I did not report re- ies in which adverse effects were found, it productive success in the pilot study (I con- failed to convey the fact that many waterbird sider it unlikely that it was reduced, because colonies continue to flourish despite inten- at least one of the pairs re-laid). In my main sive biological studies or intensive visitation. study (Nisbet 1981), I found that trapping Indeed, most readers of their paper who are adult Roseate Terns did not reduce their re- not otherwise familiar with waterbird colo- productive success relative to that of un- nies would find this fact incomprehensible. trapped controls, despite short-term effects Tables 2 and 3 in C&S listed recommen- on behavior. This study of behavior was con- dations for minimizing disturbanceby investi- ducted within an intensive field study of gators and visitors. In fact, what should be breeding biology, involving daily intrusions minimized are the adverseeffects of disturbance. into the nesting area (Nisbet et al. 1990); I Among 52 recommendations in these tables, specifically reported that reproductive suc- 43 were for restrictions on the timing, loca- cess was at least as high in my intensively tion, or manner of investigator or visitor ac- studied plots as in a low-disturbance control tivityin and around colonies; most of the rest plot (Nisbet 1981; Nisbet et al. 1990). I did were for limiting the speed or direction of not recommend that investigators should movement. None specified research activi- "avoid visiting colonies before laying is com- ties that can be carried out safely, and only plete" (as stated by C&S in their Table 2). I one specified a way in which a research activ- recommended that trapping of Roseate ity should be modified to reduce adverse Terns could be done safely after day 17 of in- effects. There was no mention of guiding vis- cubation, which necessarily requires mark- itors along boardwalks or fenced paths, and ing all study nests at the time of laying. only one mention of observation blinds. I Most of my published papers have report- am concerned that these tables and other ed intensive studies within tern colonies, in- summary statements in the paper will be cluding repeated disturbance and handling read by managers asjustifying further restric- of chicks and adults (and, in some cases, tions on access by biologists and visitors, and blood sampling or other intrusive proce- that this will have negative consequences dures). Many of my papers have explicitly both for scientific research and for the wel- addressed potential effects of research proce- fare of the birds. dures, and have stated my opinion that effects 0051110

Table 1. Studies cited by Carney and Sydeman (1999) as showing that human disturbance caused reduced productivity or breeding success in colonial waterbirds.

Study Species Reported findings and comments Giese 1996 Ad6lie Penguin Hatching success, fledging success, and productivity significantly lower in disturbed colonies, but effect Pygoscelisadeliae found only in small colonies. Ollason and Dunnett 1980 Northern Fulmar 1978, Capture of adults reduced their breeding success in same year. Research activity during hatching period Fulmarusglacialis resulted in significant reduction in colony productivity. Anderson and Keith 1980 Brown Pelican Productivity reduced relative to undisturbed subcolonies at several sites and in several years. Pelecanusoccidentalis Anderson 1988 ct Brown Pelican Productivity reduced following establishment of fishing camp on previously uninhabited island. Produc- tivity in subcolonies negatively related to distance from traces of human activity (trails, trampling, etc.). Schreiber and Risebrough 1972 Brown Pelican Hatching success lower in nests checked more frequently. Boellstorff et 1988 American White Pelican al. Productivity lower in disturbed than in control colonies after 1 or 2 visits during early stages of breeding. Pelecanuserythrorhyncus ? e Bunnell et 1981 American White al. Pelican Authors attributed low productivity in one year to low overflight by aircraft, but gave no evidence that overflight occurred, that it caused the effects, or that other factors were not involved. zv, and Reed 1981 Double-crested DesGranges Cormorant Productivity not reported. Four visits to one colony led to predation by gulls on 27% of eggs and chicks. Phalacrocoraxauritus No effect in another colony. 0 Ellison and 1978 Double-crested Cormorant Cleary Disturbance promoted gull predation and nest abandonment, but only among late-nesting groups. z Among early-nesting birds, empty nests more prevalent in disturbed plots, but in only 1 of 4 comparisons; no convincing effect on productivity (see Duffy 1979). et 1989 Double-crested Cormorant Henny al. Gull predation occurred at "a few peripheral nests" during authors' visits. Authors suggested that popu- lation shifts among islands "may be related to the changing levels of human disturbance", but gave no evidence for association of disturbance with reduced productivity. and Gochfeld 1975 Cormorants Phalacrocorax Human intrusion z Kury spp. into nesting areas made adults leave the colony, facilitating predation on eggs and H chicks by gulls. Productivity not reported. and Ellison 1979 Black-crowned Tremblay Night-Heron Visits during egg-laying or incubation resulted in nest abandonment, increased nestling mortality and re- Nycticoraxnycticorax duced productivity. Vos et 1985 Great Blue Heron Ardea herodias al. Authors reported behavioral responses only; productivity was uniformly high in 2 sites subject to con- trolled no control site. disturbances; -K Werschkul et 1976 Great Blue Heron al. Nest occupancy significantly lower in disturbed than undisturbed colonies; no difference in productivity (reported as fledglings/successful nest). et 1995a Herons Burger al. (8 species) 15-28% of chicks found dead following single intrusion by birders 3 weeks after hatching; no effect of regular visits by scientists in same colony; no effect of frequent approaches to within 50 m 0051111

Table 1. (Continued) Studies cited by Carney and Sydeman (1999) as showing that human disturbance caused reduced productivity or breeding success in colonial waterbirds.

Study Species Reported findings and comments

Anderson and Keith 1980 Heermann's Gull Productivity not measured. Ratio chicks/adults higher in subcolonies with less evidence of visitor intru- Larus heermanni sions (footprints, trash, etc.) but dates unspecified and other factors not controlled. Conover and Miller 1978 Ring-billed Gull L. delawarensis Productivity not reported. Two islands deserted following trapping of adults on incomplete clutches; no effect of trapping adults on complete clutches; no control site. Fetterolf 1983 Ring-billed Gull Chick mortality higher and productivity lower in "most"and "moderately" disturbed plots than in "least" disturbed plot. These results questioned by Brown and Morris (1994, 1995), who found no effects of dis- tr turbance in more detailed and better-controlled studies. Robert and Ralph 1975 Western Gull L. occidentalis Hatching success lower in more disturbed plot, but chick survival positively related to frequency of dis- turbance; productivity highest in most disturbed plots. Gillett et al. 1975 Glaucous-winged Gull Productivity not measured. Significantly more dead chicks found in disturbed plots, but undisturbed L. glaucescens plots were visited only at end of season. Burger 1981 Gulls, terns, skimmers Author reported effects on behavior, but none on productivity. "With several years of data... I find that reproductive success is sometimes higher and sometimes lower in completely undisturbed study areas". Nisbet 1981 Common Tern Sternahirundo, Trapping and patagial tagging did not reduce productivity in Roseate Terns; productivity not reported in Roseate Tern S. dougallii Common Terns. Burger et al. 1995a Least Tern S. antillarum Productivity lower at heavily disturbed sites (N = 52) than at infrequently disturbed sites (N = 18), but effects of disturbance not separated from effects of predation and other factors. Brubeck et al. 1981 Least Tern Productivity not reported. 40% of birds given patagial tags deserted, vs 9% of birds captured and 0% con- trols. Gochfeld 1981 Common Tern, Black Skimmer Author reported effects on behavior only, not on productivity. Rynchopsniger Safina and Burger 1983 Black Skimmer Productivity not measured; hatching success and probably fledging success reduced in subcolonies visited daily. Cairns 1980 Black Guillemot Cepphusgrylle Hatching success and productivity significantly lower in plots checked daily than in plots checked every 4 days. Piatt et al. 1980 Least and Crested Auklets Hatching success, fledging success and productivity of Least Auklets significantly lower in intensively stud- Aethia pusilla and A. cristatella ied plots than in control plots; no information on Crested Auklets. Rodway et al. 1996 Atlantic Puffin Fraterculaarctica Productivity significantly reduced in plots disturbed during incubation. Pierce and Simons 1986 Tufted Puffin E cirrhata Burrow occupancy, hatching success and productivity significantly reduced in plots disturbed during in- cubation.

Three other papers cited by Carney and Sydeman (Hockey and Hallinan 1981; Sladen and LeResche 1970; Culik et al. 1990) have not been reviewed. 0051112

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Table 2. Studies cited by Gotmark (1992) as showing that human disturbance caused reduced productivity or breed- ing success in gulls.

Study Species Reported findings and comments

Davis and Dunn 1975 Lesser Black-backed Gull Hatching success and fledging success lower in a study- Larusfuscus plot traversed twice daily than in one not so traversed, but each plot was also visited every 2 days for intensive nest-checks. Of 39 eggs lost during incubation, 15 (38%) taken by conspecifics during nest-checks. Fetterolf 1983 Ring-billed Gull See comments in Table 1. L. delawarensis

Gillett et al. 1975 Glaucous-winged Gull See comments in Table 1. L. glaucescens Kadlec and Drury 1968 Herring Gull L. argentatus 5 visits/yr on a densely occupied island "may"lower av- erage productivity by no more 0.2 young/nest; 3 metic- ulous visits/week "may"lower it by no more than 0.4 young/nest. No basis given for these conclusions; meth- ods of estimating productivity apparently differed; no undisturbed controls.

Robert and Ralph 1975 Western Gull L. occidentalis See comments in Table 1. on breeding success were minimal or absent procedures and investigator intrusions on the under the conditions of my studies (Nisbet behavior of Common Tern chicks, but did and Drury 1972; Nisbet 1981; Nisbet and Wel- not report effects on productivity. ton 1984; Nisbet et al. 1990, 1995, 1998, 1999; Many other relevant papers were not cit- Burger et al. 1995b, 1996; Galbraith et al. 1999; ed by C&S. Feare (1976) reported that inten- Nisbet and Hatch 1999; Nisbet and Spende- sive studies of Sooty Terns (Sternafuscata) low 1999). One possible exception is the involving chasing down the chicks and study by Arnold et al. (1998), in which a num- weighing them every 3 days led to increased ber of Common Tern pairs deserted their chick mortality (from about 27% to 35%), scrapes after the first egg was removed on the mostly as a result of pecking by neighboring day it was laid; however, many or most of these adults. Blokpoel (1981) reported that visits pairs moved to other scrapes and continued by researchers to colonies of Caspian Terns laying, so it is unlikely that productivitywas re- (S. caspia) and cannon-netting adults on duced. Although six of the papers cited above their nests caused desertions and losses of were published after the cut-off date for eggs or chicks to predatory gulls, but most of C&S's review, they did not refer to any of the the effects were small and are inconclusive in earlier papers, even though Burger et al. the absence of data from undisturbed con- (1995b) had repeated and extended the one trol sites. The only strong evidence for an ad- study that they did cite (Nisbet 1981). verse effect was at one site where 11/28 C&S cited only two other studies which marked nests were "deserted" following two had addressed the effects of research proce- firings of cannon-nets on one day, but even dures on terns. Brubeck et al. (1981) reported this case is unconvincing because the out- that trapping Least Terns (Sterna antillarum) come reported as "deserted" included cases at the nest caused some desertions, especially where chicks died for other reasons or dis- if patagial tags were applied. However, they persed into cover. Shugart et al. (1979) also reported that patagial tags could be applied reported on effects of cannon-netting in a to birds trapped away from the nest site with- Caspian Tern colony, but also did not use a out adverse effects, and that effects of trap- control site; they found no effect of a single ping and tagging were minimal at a site where firing in 1976, but 65% of nests were "desert- the birds were habituated to human activity. ed" following five firings in three days in Gochfeld (1981) reported effects of research 1977. Hill and Talent (1990) reported that 0051113

320 WATERBIRDS trapping and banding Least Terns and at- that Sandwich Tern (S. sandvicensis) chicks taching radio transmitters did not signifi- dispersed awayfrom their nests about one day cantly affect reproduction. Becker and Finck earlier in a disturbed colony than in undis- (1991), Klaassen et al. (1992) and Frank and turbed colony, but did not report any effect Sudmann (1993) reported that radio trans- on chick survival. Fetterolf and Blokpoel mitters did not affect behavior, nest atten- (1983) reported that hatching success in a col- dance, chick growth, breeding success, or ony of Caspian Terns was significantly higher energy expenditure in Common Terns. Mor- in 1980 and 1981, when late nests were ob- ris and Burness (1992) similarly found that served remotely without intrusion into the attaching radio transmitters to Common nesting area, than in 1979, when all nests were Terns did not affect nest attendance or chick visited every 1-3 days. However, the actual data feeding rates. Uttley et al. (1994) reported suggest that this difference was caused by oth- that one pair of Arctic Terns (S. paradisaea) er factors. The difference was also observed that was trapped, injected with doubly-la- among early nests (which were disturbed sim- beled water, held for one hour in a cloth bag, ilarly through hatching); hatching success in and subjected to blood sampling deserted 1980 and 1981 was similar in visited and unvis- their nest, but that others trapped and inject- ited nests; among late nests, hatching success ed did not do so. Flint and Nagy (1984) had was higher in visited than in unvisited nests. earlier reported no adverse effects among Same-year controls were not used. Quinn Sooty Terns studied by the same method, (1984) reported that Ring-billed Gulls (Larus and Galbraith et al. (1999) found no adverse delawarensis)took Caspian Tern eggs during effects on Common Terns. Wendeln and nest-checks. Covering the nests during nest- Becker (1996) reported that spraying dyes checks reduced egg-losses from 31% in 1978 onto incubating Common Terns did not af- to 12% in 1979, but same-year controls were fect their behavior, social interactions, or not used and productivity was not measured. overwinter survival. Becker and Wendeln Morrison (1996) found that investigator in- (1997) reported that implanting transpon- trusions, including intensive nest studies, had ders into Common Terns did not affect their no effects on breeding success of Arctic or behavior, but did not report comparative Common Terns. Blanco et al. (1999) found data on treated and control birds. Zingo that hatching success in South American (1998) reported a series of studies of the ef- Terns (Sternahirundinacea) was similar at visit- fects of trapping Roseate Terns on their be- ed and unvisited nests, despite the presence havior and reproductive success, including and activity of mammalian predators; they detailed comparisons with untrapped birds. suggested that investigator activity might be Trapping appeared to increase the frequen- beneficial to the terns by disturbing preda- cy of nest desertion in one year when food tors. Shealer and Haverland (2000) found was limiting, but not in other years. Growth that investigator intrusions, including inten- rates were slightly lower in the chicks of par- sive nest studies, had no effects on breeding ents that had been trapped, but the effect success of Black Terns (Chlidoniasniger). Buck- was transitory and there was no measurable ley and Buckley (1972) referred to Royal effect on chick survival or mass at fledging. Terns (Sterna maxima) abandoning colony- sites when subjected to "disturbance"during but this was disturbance Investigator Intrusions egg-laying, by preda- tors; Royal Terns tolerated intensive work by Only a few papers have reported effects of the authors throughout the egg-laying period. investigator intrusions on nesting terns, and none of these was cited by C&S. Domm and Visitor Intrusions Recher (1973) attributed breeding failure in Roseate Terns to investigator intrusions, but C&S cited three papers that had ad- Hulsman (1977) attributed a similar event at dressed effects of visitor intrusions on terns. the same site to predation. Veen (1977) found Erwin (1980) concluded that Common 0051114

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Terns were excluded from preferred nesting panded into disturbed areas, despite heavy sites on barrier beaches in New Jersey by and increasing tourist use (80,000 visitors/ human activity and development, and were year) throughoutthe breeding season. further excluded from alternative sites on islands Gulls dredge spoil by Herring (Larus VisitorApproaches argentatus),so that they nested primarily in salt marshes. The reference area was coastal C&S cited three papers that had ad- Virginia, where human activity and develop- dressed effects of visitor approaches on ment were restricted and Common Terns terns. Burger et al. (1995a) reported that nested mainly on barrier beaches. C&S (Ta- breeding success of LeastTerns was lower at ble 1) cited this as a study of the effect of hu- disturbedthan undisturbedsites in NewJer- man disturbance on "breeding population sey, and was especiallylow at sites disturbed size trends", but it did not show such an ef- by ecotourists(birdwatchers). However, they fect and Erwin did not present it as such. Nor also reported that breeding success at these does it suggest an effect on breeding success sites was affected by predators,flood tides, or productivity,because Common Terns are at and heavy rains; they offered no evidence least as successful on marsh sites as on beach that it wasaffected by human disturbancein- sites in New Jersey (Burger and Gochfeld dependently of these other factors. Erwin 1991: Fig. 9.1). Also, Erwin's study showed (1989) reportedflushing distancesfor three that Least Terns nested mainly on barrier species of terns at 30 colony sites in Virginia beach sites in NewJersey and were much less and North Carolina. Rodgers and Smith numerous in Virginia (opposite to the differ- (1995) reported flushing distancesfor Least ence reported for Common Terns). Finally, Ternsat two colonies in Florida.In addition Erwin did not distinguish between putative to these three papers,Siebolts (1998) report- effects of human disturbance and develop- ed flight responsesof CommonTerns to visi- ment. Burger (1981) reported no informa- tor approachesat three colonies in Germany. tion on terns. Barnes and Hill (1989) reported None of the lastthree studies, however, investi- that large numbers of Black Noddies (Anous gatedor reportedeffects on breedingsuccess. minutus) had recently colonized the western half of Heron its Island, Australia, despite Other Typesof Disturbance occupation by a resort and a research sta- tion, but they did not describe the nature of Burger (1998) reported flight responses the disturbance or measure its effects. Hill of breeding Common Terns in response to and Rosier (1989) noted that the nesting movementsof motorboatsand personalwa- density was as high in the developed area as tercraft,but did not investigateeffects on re- in the undeveloped area. They also stated productive success. Although many tern that Roseate Terns no longer nested on the colonies are activelyprotected and managed, island, which they attributed to develop- I have found no studies of effects of distur- ment, but gave no reason for this conclusion. bance incidental to positive management. Two other reports on visitor intrusions Managementis generallyregarded as benefi- were not cited by C&S. Burger and Gochfeld cial to terns (e.g., Burger et al. 1995a;Kress (1991, pp. 322-323) stated that human dis- 1997), so any adverseeffects of disturbance turbance was responsible for 35% of colony are presumablyoutweighed by positive ef- failures among Common Terns on beach fects of management.I have found no pub- sites in New Jersey, but was unimportant at lished reports of negative management of salt marsh sites in NewJersey or in salt marsh terns. Harassment and vandalism are often or beach sites in New York. However, they said to have adverse effects on terns, but I did not give the basis for these conclusions. have found no published descriptions. Feare Dunlop (1996) reported that Bridled Terns (1976) reported on the effects of egging (Sternaanaethetus) had increased in numbers (egg-harvesting) on Sooty Terns in the Sey- on Penguin Island, W. Australia, and had ex- chelles Islands, and made recommendations 0051115

322 WATERBIRDS for harvesting quotas and schedules that ductive success in terns, and their recom- would not have adverse effects on population mendations (Table 2) that investigators maintenance. In a small experimental study should avoid approaching colonies and designed to simulate effects of egging, he should enter them only during limited peri- found that at least half the pairs whose eggs ods of the nesting cycle. were removed re-laid, but that breeding suc- Likewise, the studies cited above provide cess was lower from the replacement clutch- no definitive evidence that visitor intrusions es. Tern eggs are taken in numbers in many or visitor approaches cause adverse effects developing countries (Feare 1984; Burger (breeding failure, colony desertion, or colo- and Gochfeld 1994), but there have been few ny displacement) on breeding terns. The published reports on this in recent decades. most compelling evidence that they do is provided by the studies of Erwin (1980), and Gochfeld (1991) and et Summary: Reported Effects of Human Burger Burger Disturbance on Terns al. (1995a), but none of these studies exclud- ed alternative causal explanations. The papers cited in this section include a In summary, there is no substantial evi- few records of terns deserting their nests in dence in the scientific literature that human response to the most intrusive research pro- disturbance affects reproductive success or cedures (e.g., patagial tagging, trapping ear- colony site occupation among terns. Review- ly in incubation, injection with doubly- ers agree that human disturbance may have labeled water, or repeated cannon-netting these effects, but few actual cases have been over nests). However, in all these cases terns reported in the scientific literature, even an- of the same species have tolerated the same ecdotally. It is true that in eastern North procedures when conducted in less intrusive America breeding terns tend to concentrate ways. Even in the cases where desertions oc- at sites where human disturbance is least and curred, it is not clear that productivity was where disturbance is limited by protection significantly reduced, because at least some and management (e.g., Erwin 1980; Burger of the birds re-laid in the same seasons (e.g., and Gochfeld 1991; Nisbet and Spendelow Shugart et al. 1979; Arnold et al. 1998). 1999). However, many of the same sites were The only case where a significant adverse occupied by terns 100 or more years ago, be- effect (lowered breeding success) has been fore present-day patterns of human distur- attributed to intensive research is that of bance were established (Smith 1884; Stone Feare (1976); that effect was small and could 1894; Norton 1913; Bent 1921; Murray 1952; have been reduced or eliminated by fencing Nisbet 1973). Thus, the distribution of terns in the study chicks. The only report of an ad- among colony sites in eastern North Ameri- verse effect of investigator intrusions is that ca can be explained at least as well as result- of Domm and Recher (1973), but this report ing from avoidance of predation as from was anecdotal and did not exclude effects of avoidance of human disturbance (Nisbet other factors. Even if this effect was caused and Spendelow 1999). Predation and hu- by investigator intrusion, it could have been man disturbance tend to co-occur, both be- averted by making visits later in the nesting cause each is more prevalent at sites close to cycle. Hence, I conclude that, with modest or accessible from the mainland, and be- precautions, most or all species of terns can cause many of the predators are human be studied-in some cases intensively and in- commensals (Nisbet and Spendelow 1999). trusively-without significant adverse ef- Hence, the association of tern colonies with fects. This statement is not intended to sites that are actively protected and managed advocate uncontrolled intrusion into unhab- is as likely to result from protection following ituated colonies and immediate use of intru- the terns as vice versa.It is certainly likely that sive techniques (see below), but is intended human disturbance prevents terns from to rebut C&S's conclusory statement (p. 71) forming new colonies on barrier beaches that investigator disturbance reduces repro- and inshore islands in eastern North Ameri- 0051116

DISTURBANCE,HABITUATION AND MANAGEMENT 323 ca, but such sites are not favorable for terns man disturbance have been reported fre- under present-day conditions because of high quently in terns and have been interpreted levels of predation (Burger and Gochfeld as resulting from habituation (e.g., Bretsch 1991; Nisbet and Spendelow 1999). 1926; Cullen 1956; Nisbet 1977; Gochfeld Nevertheless, I believe that actual effects 1978; Dunlop 1996). of human disturbance on terns are probably In my own studies of Common and Rose- occurring but are under-reported in the sci- ate Terns, I have systematicallypromoted tol- entific literature. I know of many unpub- erance at each of my study sites by lished, anecdotal accounts of tern colonies progressivelyescalating the intensity of distur- reportedly subjected to human intrusion, ha- bance, testing each new research technique rassment, or vandalism. Most of these re- on a few individuals before extending it to ports refer to Least Terns or Little Terns others, observing responses to intrusions, and (Sterna albifrons)nesting on barrier beaches withdrawing as soon as the terns' responses in North America or Europe. These reports appeared potentially harmful to eggs or are commonly made orally in meetings of chicks. I arrange my work schedules so that tern wardens or managers, but rarely, if ever, each study-plotor area within the colony is dis- are published. Even if they were submitted turbed for no more than 20-30 minutes at a for publication, most of them are anecdotal time, but that each is visited at least once and and would not withstand critical review for usually several times each day. Because Rose- scientific journals. Because Least and Little ate Terns appeared initially less tolerant than Terns are subject also to predation and many Commons (Nisbet 1981), I tested each new re- other adverse factors (Burger et al. 1995a), a search procedure on Commons and estab- scientifically defensible conclusion that they lished that it was not harmful before testing it are affected significantly by human distur- on Roseates. Although I did not measure tol- bance or vandalism would require critical erance to disturbance precisely in either spe- studies comparing disturbed and reference cies, Common Terns showed clear signs of colonies. Because the human activities that increasing tolerance at each study site by the are thought to have adverse effects are spo- middle of the second year of study and Rose- radic, unpredictable, and difficult to ob- ates by the middle of the third. In each spe- serve, such studies would be difficult to carry cies, tolerance has increased continuously out. Because such studies would require with the duration of study. By the 30th year of managerial resources that are usually devot- study,most Common Terns allow approach to ed to preventing human disturbance, they within 10 m before flying off their nests, and are unlikely to be performed. return to their nests or chicks at ranges of 1-2 m within a few seconds after I or my assistants Habituation and Tolerance in Terns sit down. Some individuals can be touched on the nest, and others stand on our heads or I have found no formal studies of habitu- shoulders while we work on their neighbors. ation in terns (i.e., longitudinal studies of Common Terns ignore trapping of their the same birds or groups comparing toler- neighbors, and most trapped birds return to ance levels after varying durations of distur- their nests within a few minutes, even after bance). The nearest approach to such a drawing blood or other intrusive procedures. study is an experimental simulation by Roseate Terns still are less tolerant than Com- Wi-rm and Huppop (1998), who found that mon Terns, but most return to their nests heart rates of Common Terns increased within 5 m of us when we sit down, and a few when recorded sounds associated with dis- now peck our heads or fingers. Terns nesting turbance (alarm calls of terns or shorebirds, for the first time are almost as tolerant as old- or aircraft noise) were played to them, but er birds. Among Roseate Terns, prospecting that the responses declined in intensity after birds (2 years old) can be identified by read- the stimulus was repeated about 20 times. ing field-readable bands (Nisbet and Spende- High tolerance levels to various types of hu- low 1999): these birds are as tolerant of close 0051117

324 WATERBIRDS approach as breeders when loafing and court- nesting in Puerto Rico allowed approach to ing on the edge of the colony (unpubl. data). within 1 m before leaving their nests (Burger Common Tern chicks initially flee when ap- and Gochfeld 1988). proached, but become more tolerant within Terns also become tolerant to heavy vehi- 5-10 days and subsequently stand within 3 m cle or boat traffic. Common Terns in New of us and solicit food from their parents. Be- York ignored heavy boat traffic within a few cause only a small fraction of the birds in the m of their nests (Bretsch 1926). Least Terns colony fly off their nests in response to our ac- commonly nest on roofs in the southern tivityat any one time, we are able to work con- USA (Krogh and Schweitzer 1999 and refer- tinuously, moving steadily through the ences therein). At Portland, TX, Least Terns nesting area so that no individual birds stay off nested within 5 m of a busy highway their nests or chicks for more than a few min- (Brubeck et al. 1981). In The Netherlands, utes. An important consequence of the in- Common Terns not only nested on roofs but creased tolerance of the birds of the activityof also on a traffic roundabout on a busy high- biologists is that they have also become toler- way (Bouwmeester and Van Dijk 1991). ant to the presence and activity of other visi- tors. Many visitors to the island can watch the OTHER COLONIALWATERBIRDS terns feeding chicks from ranges down to 3 m without disturbing them, or can walk through I have not reviewed published data on the breeding area on fenced paths without other species of colonial waterbirds in as disturbing individual birds for more than a much detail as data on terns. Readily avail- few seconds. able data (Table 1) indicate adverse effects There are many other reports of high tol- of human disturbance on several species of erance of breeding terns to human activity. colonial waterbirds. Species in which adverse Most colonies of Roseate Terns in the north- effects have been convincingly documented eastern USA have been studied by biologists include pelicans (Pelecanusspp.: Schreiber and for many years, and the birds have become Risebrough 1972; Johnson and Sloan 1976; (to various degrees) tolerant of the presence Anderson and Keith 1980; Boellstorff et al. and activity of biologists (Nisbet and Spend- 1988), Double-crested Cormorants (Phala- elow 1999). Common Terns at the same and crocoraxauritus: Kury and Gochfeld 1975), other sites have become even more tolerant Greater Flamingo (Phoenicopterusruber. Bou- (personal observations). At several sites, tin and Cherain 1989), alcids (Piatt et al. 1980; terns nest unconcernedly within a few m of Harris and Wanless 1984; Pierce and Simons busy beaches (e.g., Common Terns in New 1986; Rodway et al. 1996), and Adelie Pen- York: Gochfeld 1978; Least Terns in Califor- guins (Pygoscelisadeliae: Giese 1996). Howev- nia: Massey 1981; Minsky 1987; and Texas: er, there is little evidence for significant Brubeck et al. 1981), or allow visitors to walk effects on productivity in gulls or herons (Ta- through the nesting area on fenced paths or bles 1 and 2; see also Harris 1964; Goehring boardwalks (e.g., Arctic and Common Terns and Cherry 1971; Frederick and Collopy at the Farne Is, UK: Cullen 1956, and Mach- 1979; Parsons and Burger 1983; Burger and ias Seal Is., Canada: Morrison 1996; Bridled Gochfeld 1983; Bergmann 1986; Mueller and Terns at Penguin Island, W. Australia: Dun- Glass 1988; Brown and Morris 1994, 1995). lop 1996). Royal Terns in Virginia tolerate bi- Gotmark (1992) listed five studies of gulls as ologists within the nesting area and tend showing adverse effects of investigator dis- their chicks within 3 m so long as the biolo- turbance, but I regard most of these studies gists sit down (P. A. Buckley, pers. comm.). as inadequate and inconclusive (Table 2). The Least Terns nesting at a busy beach and pub- resistance of gulls and herons to human dis- lic park in Texas appeared more tolerant of turbance is underlined by the difficulty that trapping and tagging than birds from less managers have experienced in trying to elim- disturbed sites (Brubeck et al. 1981). Sooty inate colonies or reduce numbers by harass- Terns and Brown Noddies (Anous stolidus) ment and egg-breaking alone, without killing 0051118

DISTURBANCE,HABITUATION AND MANAGEMENT 325 adults (e.g., Telfair and Thompson 1986; low tolerance observed in many colonies at Ickes et al. 1998; Olijnik and Brown 1999). the present day is an acquired response to In several studies, significant effects were human predation in the past. If this interpre- noted when disturbance occurred during egg- tation is correct, the low tolerance should be laying or early incubation, but were smaller reversible by repeated experience of benign or absent when disturbance occurred later human disturbance in the future. in the nesting cycle (Conover and Miller 1978; Ellison and Cleary 1978; Tremblay and CONCLUSIONS Ellison 1979; Pierce and Simons 1986; Rod- way et al. 1996). In several cases, adverse ef- Based on the material that I have re- fects were mediated by gulls or other viewed for this Commentary, I draw the fol- predators, which took eggs or chicks when lowing conclusions: nesting birds of other species were displaced 1. Much of the literature on human dis- from their nests or broods by investigator in- turbance and colonial waterbirds has been trusions or visitor intrusions (Davis and of low scientific quality, with ill-defined con- Dunn 1976; Ellison and Cleary 1978; Ander- cepts and terms, poorly-framed questions, son and Keith 1980; Drapeau et al. 1984; reliance upon anecdote and correlation, Ahlund and G6tmark 1989; Jewell and Ban- and poorly-controlled observational studies. croft 1991). Some reviews and summaries have been un- Tolerance to human disturbance and/or critical and focused upon putative adverse habituation have been reported in many spe- effects, with inadequate consideration of po- cies. I have observed highly tolerant colonies tential positive effects of human activity, in- of gulls in the UK, USA and Australia, pen- cluding habituation. Similar conclusions guins in Australia and Argentina, storks in were presented by Nimon and Stonehouse Europe, USA and Thailand, frigatebirds and (1995), from a review of the literature on pelicans in the Caribbean. At Punta Tombo, Antarctic Penguins: Argentina, Magellanic Penguins (Spheniscus Many years' research on breeding and magellanicus)tolerate large numbers of visi- population studies of Antarctic Pen- tors walking among the nests and suffer no guins has left us with little concept of adverse effects, despite the documentation what constitutes significant human of physiological (Yorio and Boers- responses disturbance, and how it be ma 1992; Hood and Boersma 1998; Walker et might monitored and controlled.... At this al. 1999; P. D. Boersma, pers. comm.). Paul stage of inquiry, it is necessary to de- and Amget (1992) described three mixed fine the questions which researchers colonies of wading birds Storks (Open-billed must address, and it is to Anastomus oscitans,cormorants and possible herons) make which be im- at sites in suggestions may protected (monasteries) Thailand; in such birds humans, vehicles and portant answering questions. nesting ignore The answers themselves await further dogs immediately under the nests. Grubb investigation. (1979) described an urban colony of herons that was highly tolerant of boat and aircraft 2. Demonstration of causal relationships traffic nearby. "Nuisance" heronries, estab- between human disturbance and adverse ef- lished in urban or suburban areas, have be- fects on colonial waterbirds (effects on come an increasing problem in the USA in breeding success, survival, or colony occupa- recent years (Taylor et al. 1982; Telfair and tion) is inherently difficult. The main prob- Thompson 1986). The high tolerance of sea- lem is that these characteristics of colonial birds nesting at remote oceanic islands or in waterbirds are influenced by many other fac- the Antarctic to visitor approaches and intru- tors, including predation, weather, flooding, sions is legendary (e.g., Humphrey et al. food availability, and competition. As most 1987). This suggests that high tolerance is a waterbird biologists know, it is very difficult "natural"state in many seabirds and that the to measure the effects of any of these factors 0051119

326 WATERBIRDS while controllingforvariability in the others.The events are single incidents, they constitute same difficulties arise in documenting the ef- little more than anecdotes. Even in cases fects of human disturbance, except that dis- where events are numerous enough to sup- turbance is often more difficult to measure. port statements about frequency (e.g., Burg- 3. Documentation of effects of investiga- er and Gochfeld 1991), major questions tor activity is especially difficult, because remain about documentation of cause-effect measurement of breeding success or survival relationships (see point 2 above). requires intrusion into the breeding area 6. For terns, I have found little scientifi- and usually requires handling and marking cally acceptable evidence that human distur- individual birds. Hence, it is very difficult to bance cause substantial adverse effects on compare the performance of disturbed and breeding success, survival, or colony occupa- undisturbed birds without using different tion. I suspect (a) that egging has had and methods (see, for example, comments on continues to have adverse effects on terns in Gillett et al. 1975 in Table 1; also Burger 1981). developing countries, and (b) that occasion- 4. It is easier to use rigorous methods to al incidents of intrusion, harassment or van- determine the effects of research proce- dalism have adverse effects on terns in dures, but this provides only limited infor- developed countries, but no convincing cases mation about the effects of other types of have been reported in the scientific literature. human disturbance. Several studies have 7. Convincing evidence of adverse effects shown adverse effects of extremely intrusive of human disturbance have been reported research procedures. However, most of these for several species and groups of colonial studies were designed to identify less intru- waterbirds, including penguins, flamingos, sive procedures that would not cause adverse pelicans, cormorants, and alcids. Most of the effects, and most succeeded in doing so. effects that have been documented convinc- Many of these studies show that, with reason- ingly resulted from disturbance early in the able precautions, colonial waterbirds toler- nesting cycle, from promotion of predation ate quite intrusive procedures (trapping, by gulls or other species, or both. color-marking, drawing blood, injecting 8. Contrary to prevailing opinions, there transponders or doubly-labeled water, at- is little or no scientifically acceptable evi- taching radio transmitters, etc.). The impor- dence that gulls or herons are substantially tance of these findings in the present affected by human disturbance. context is that they place limits on the possi- 9. In my opinion, reported "effects" of ble effects of investigator intrusions. For ex- human disturbance on behavior or physiolo- ample, it is not plausible that terns could be gy of colonial waterbirds have very little rele- significantly affected by investigator intru- vance or cogency. No evidence has been sions into the nesting area without handling, presented that any of these "effects"result in if they are not significantly affected by inves- reductions in breeding success, survival, or tigator intrusions into the nesting area com- colony occupation. In particular, there is no bined with trapping, injection with doubly- scientific evidence that upflights, or "flush- labeled water, drawing blood, and attach- ing", are adverse effects, except in circum- ment of radio transmitters (Becker and stances where they allow predators to gain Finck 1991; Klaassen et al. 1992; Frank and access to eggs or chicks. Sudmann 1993). 10. Most or all species of colonial water- 5. Effects of visitors (non-investigators) birds are capable of developing tolerance are extremely difficult to study, because their ("habituation") to human distur-bance. Al- activities are extremely variable, sporadic, though habituation has not been demon- usually unpredictable and often unobserved. strated formally through longitudinal Although it is likely that visitors do cause ad- studies of the same individuals, groups, or verse effects on colonial waterbirds, very few colonies, high tolerance has been reported convincing cases have been reported in the in many species, including representatives of scientific literature. Because most reported most major groups of colonial waterbirds. 0051120

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MANAGEMENTRECOMMENDATIONS management: the first to enforce the regula- tions preventing human access, the second 1. One of the major purposes of this to train the birds to tolerate human presence Commentary is to challenge the mind-set and to manage visitors to behave in predict- (e.g., G6tmark 1992; Carney and Sydeman able ways. One problem with the first option 1999) that the effects of human disturbance is that any failure of enforcement will lead to are always"adverse". This mind-set has led to unsupervised human intrusion into a colony the general principle of management that of birds that has low tolerance. Another disturbance to waterbird colonies should be problem with the first option is that most minimized, except perhaps as part of a trade- management plans require occasional intru- off against other benefits. This Commentary sion of managers to count nests, measure argues that human disturbance is not always productivity, and monitor for predation. For adverse, and that what should be minimized many species of colonial waterbirds, this are the adverseeffects of disturbance. management protocol of minimizing human 2. The phenomenon of habituation (or disturbance, except for sporadic visits by increase in tolerance, which is what is usually managers, is likely to maximizethe probabili- measured) means that birds' behavioral re- ty of adverse effects. For this reason, I recom- sponses are not linearly or even monotoni- mend that, wherever possible, waterbird cally related to the intensity and frequency of colonies should be managed to promote ha- disturbance. The initial response of unhabit- bituation. This can only be achieved with the uated birds to human intrusion (physiologi- frequent presence of wardens or monitors cal stress responses, upflights, or fleeing) (although it is not necessary for these to be reflects their perception of the threat posed present continuously or even every day). by human intruders and may lead to adverse The unorthodox part of my recommenda- effects on breeding success or colony occu- tion is that these wardens or monitors should pation. Beyond a certain point, however, be trained not to stay out of the colony, but physiological responses and upflights form to disturbit frequently, regularly, and predictably. part of the process through which the birds 4. Consistency and predictability are learn that human intrusions are not threat- important elements in the process of habitu- ening. The relationship between responses ation. To the extent possible, wardens, man- and adverse effects is then reversed. The agers, researchers and visitors should behave more the birds become habituated to hu- in the same ways, including approaching man intrusions, the less they are likely to be and walking through the colony along the affected adversely by the next intrusion (see same tracks. Provision of fenced paths or Robert and Ralph 1975 for a documented boardwalks through a colony is an excellent example). Specifically, as birds become ha- way to manage visitors and simultaneously to bituated to regular, predictable intrusions promote tolerance (Dunlop 1996). by biologists or managers, they become 5. Managers should understand that the more able to tolerate occasional uncon- scientific basis for managing human distur- trolled intrusions by visitors (USFWS 1998). bance in waterbird colonies is tenuous, be- Beyond this point, therefore, disturbance cause most scientific studies of the effects of should be maximized,not minimized. disturbance have yielded inconclusive re- 3. In principle, there are two ways to min- sults (see previous section). In the past, this imize the adverseeffects of human disturbance understanding has been used, invoking the on colonial waterbirds. One is to forbid all "precautionary principle", to justify minimiz- human access, so that the birds can breed ing human access to waterbird colonies. This successfully without any disturbance. The Commentary argues that the "precautionary other is actively to promote habituation, so principle" is much more complicated in this that the birds learn to tolerate human pres- case (see points 2 and 3 above). In particular, ence and breed successfully in spite of con- because the relationship between distur- stant human activity. Both require active bance and adverse effects may be either pos- 0051121

328 WATERBIRDS itive or negative (point 2 above), it is not its potential adverse effects. They need to be immediately obvious whether and in what trained to observe the responses of birds to circumstances the "precautionary principle" their activities and to monitor the lengths of requires either minimizing or maximizing upflights and absences, especially in hot or disturbance of various kinds. Hence, rational wet weather or in the presence of predators. management of waterbird colonies will con- Information should also be made available to tinue to require good judgment based on managers, so that they can write permit con- knowledge and understanding of the species ditions that will not be either over- or under- and locations involved, rather than any gen- restrictive. Most available guidelines for the eral principle to minimize human access. conduct of research are insufficiently de- 6. Waterbird colonies can be important tailed. I recommend that experienced re- scientific resources (as sites for research) and searchers should prepare detailed, species- educational or recreational resources (as sites specific guidelines that can be used as part of for showing wildlife to students or the general the training of inexperienced people. public). There are many good examples of the use ofwaterbird colonies for both purpos- RESEARCH NEEDS es (e.g., Dunlop 1996; Wendeln and Becker of visitor 1998). However, many management plans ex- 1. Reports on apparent effects of clude or restrict such uses. In my opinion, the intrusions, harassment, and vandalism and promotion of habituation of waterbird colo- waterbird colonies should be compiled nies will not only be beneficial to the conser- summarized. Although individual cases can a of vation of the bird populations, but will permit be dismissed as anecdotal, collection useful infor- and promote beneficial multiple uses. available reports might provide 7. All these recommendations must be mation on patterns of occurrence or cause- tempered in cases where colonies are subject effect relationships. Protocols should be devised for to predation by diurnal avian predators such 2. rig- as gulls or crows. Most of the convincing cas- orous testing of hypotheses about effects of intru- es of human disturbance causing adverse ef- research procedures and investigator fects on colonial waterbirds (including those sions on colonial waterbirds. com- in Table 1) were mediated through the pro- 3. Studies should be designed to of different motion of predation by these species. Al- pare the effectiveness manage- or though promotion of tolerance is especially ment techniques (e.g., excluding visitors, desirable in these circumstances (see Rec- managing for multiple use with maximum ommendation 3), it is not clear that it can access for visitors). always be achieved; it will certainly require extreme care to avoid damaging predation ACKNOWLEDGMENTS early in the process. I recommend that exper- iments should be done with vulnerable I thank Dee Boersma, Paul Buckley, Kate Devlin, spe- Nick Dunlop, Alan Johnson, Ian Jones, Rich Paul, Jim cies such as cormorants or pelicans, to Quinn, Dave Shealer, and Jeff Spendelow for useful in- determine whether tolerance can be pro- formation, and Jeremy Hatch for comments on the moted by repeated approaches towards the manuscript. nesting area, without coming close enough LITERATURECITED to cause lengthy upflights. 8. Because human disturbance clearly has Ahlund, M. and F. G6tmark. 1989. Gull predation on Ei- the potential to cause adverse effects, both der ducklings Somateriamollissima: effects of human researchers and wardens should be trained disturbance. Biological Conservation 48: 115-127. Anderson, D. W. and J. O. Keith. 1980. The human in- to recognize this potential and to act in ap- fluence on seabird nesting success: conservation im- propriate ways. I have found that some re- plications. Biological Conservation 18: 65-80. searchers and students who enter waterbird Arnold, J. A., I. C. T. Nisbet and J. J. Hatch. 1998. Are Common Terns really indeterminate layers? Re- colonies for the first time are remarkably in- sponses to experimental egg removal. Colonial sensitive to the disturbance they cause and to Waterbirds 21: 81-86. 0051122

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Barnes, A. and G. E. Hill. 1989. Census and distribution Burger, J. and M. Gochfeld. 1991. Reproductive vulner- of Black Noddy Anous minutus on Heron Island, ability: parental attendance around hatching in Ro- November 1985. Emu 89: 129-134. seate (Sterna dougallii) and Common (S. hirundo) Becker, P. H. and P. Finck. 1991. Funkpeilung von Terns. Condor 93: 125-129. Flussseeschwalben (Sterna hirundo) im Wattenmeer. Burger, J. and M. Gochfeld. 1991. The Common Tern: Seev6gel, Zeitschrift Verein Jordsand 12: 52-61. Its breeding biology and social behavior. Columbia Becker, P. H. and H. Wendeln. 1997. A new application University Press, New York. for transponders in population ecology of the Com- Burger,J. and M. Gochfeld. 1994. Predation and effects mon Tern. Condor 99: 534-537. of humans on island-nesting seabirds. Pp. 39-67 in Bent. A. C. 1921. Life histories of North American gulls Seabirds on islands: Threats, case studies and action and terns. U.S. National Museum Bulletin 113: 1-345. plans (D. Nettleship, J. Burger and M. Gochfeld, Bergmann, G. 1986. Feeding habits, accommodation Eds.). BirdLife Conservation Series No. 1. BirdLife to man, breeding success and aspects of coloniality International, Cambridge, UK. in the Common Gull Larus canus. Ornis Fennica Burger, J., M. Gochfeld and L. J. Niles. 1995a. Eco- 63: 65-78. tourism and birds in coastal NewJersey: contrasting Blanco, G., P. Yorio and M. Bertellotti. 1999. Effects of responses of birds, tourists, and managers. Environ- research activity on hatching success in a colony of mental Conservation 22: 56-65. South American Terns. Waterbirds 22: 148-150. Burger, J., I. C. T. Nisbet, C. Safina and M. Gochfeld. Blokpoel, H. 1981. An attempt to evaluate the impact of 1996. Temporal patterns of reproductive success in cannon-netting in Caspian Tern colonies. Colonial the endangered Roseate Tern (Sternadougallii) nest- Waterbirds 4: 61-67. ing on Long Island, New York, and Bird Island, Mas- Boellstorff, D. E., D. W. Anderson, H. M. Ohlendorf and sachusetts. Auk 113: 131-142. E. J. O'Neill. 1988. Reproductive effects of nesting Burger, J., I. C. T. Nisbet, J. M. Zingo, J. A. Spendelow, studies in an American White Pelican colony. Colo- C. Safina and M. Gochfeld. 1995b. Colony differen- nial Waterbirds 11: 215-219. ces in response to trapping in Roseate Terns. Con- Boutin, J. and Y Cherain. 1989. Compte rendu orni- dor 97: 263-266. thologique camarguais pour les annees 1986-1987. Cairns, D. 1980. Nesting density, habitat structure and Revue d'Ecologie 44: 165-189. human disturbance as factors in Black Guillemot re- Bouwmeester, J. and J. van Dijk. 1991. Broedende Visdi- production. Wilson Bulletin 92: 352-361. even Sterna hirundoop het dak van de bloemenveil- Carney,J. M. and W. J. Sydeman. 1999. A review of hu- ing Aalsmeer. [Roof-nesting of Common Tern Sterna man disturbance effects on nesting colonial water- hirundo at Aalsmeer.] Limosa 64: 25-26. [In Dutch birds. Waterbirds 22: 68-79. with English summary.] Conover, M. R. and D. E. Miller. 1978. Reactions of Ring- Bretsch, C. 1926. Nesting of the Common Tern at Thou- billed Gulls to predators and human disturbances at sand Islands, Jefferson County, New York. Wilson their breeding colonies. Proceedings of the 1978 Bulletin 36: 200-201. Conference of the Colonial Waterbird Group 2: 41- Brown, K. M. and Morris, R. D. 1994. The influence of 47. investigator disturbance on the breeding success of Culik, B., D. Adelung and A.J. Woakes. 1990. The effect Ring-billed Gulls (Larus delawarensis). Colonial of disturbance on the heart rate and behaviour of Waterbirds 17: 7-17. Adelie Penguins (Pygoscelisadeliae) during the breed- Brown, K. M. and Morris, R. D. 1995. Investigator distur- ing season. Pages 177-182 in Antarctic ecosystems: bance, chick movement, and aggressive behavior in Ecological change and conservation (K. R. Kerry and Ring-billed Gulls. Wilson Bulletin 107: 140-152. G. Hempel, Eds.). Springer Verlag, Berlin, Germany. Brubeck, M. V., B. C. Thompson and R. D. Slack. 1981. Cullen,J. M. 1956. A study of the behaviour of the Arctic The effects of trapping, banding, and patagial tag- Tern (Sterna macrura). D.Phil. Thesis, University of ging on the parental behavior of Least Terns in Tex- Oxford, Oxford, UK. as. Colonial Waterbirds 4: 54-60. Davis,J. W. F. and E. K. Dunn. 1976. Interspecific preda- Buckley, F. G. and P. A. Buckley. 1972. The breeding tion and colonial breeding in Lesser Black-backed ecology of Royal Terns Sterna (=Thalasseus)maxima Gulls Larusfuscus. Ibis 118: 65-77. maxima.Ibis 114: 344-359. DesGranges,J. and A. Reed. 1981. Disturbance and con- Bunnell, F. L., D. Dunbar, L. Koza and G. 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Human disturbance and breeding birds. es to human intruders of Herring Gulls (Larus argen- Auk 96: 815-816. tatus) and Great Black-backed Gulls (L. marinus) Dunlop, J. N. 1996. Habituation to human disturbance with varying exposure to human disturbance. Behav- by breeding Bridled Terns Sternaanaethetus. Corella ioural Processes 8: 327-344. 20: 13-16. Burger,J. and M. Gochfeld. 1988. Defensive aggression Ellison, L. N. and L. Cleary. 1978. Effects of human dis- in terns: effect of species, density and isolation. Ag- turbance on breeding of Double-crested Cormo- gressive Behavior 14:169-178. rants. Auk 95: 510-517. 0051123

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