Nest Predation and Nest Sites

Thomas E. Martin

BioScience, Vol. 43, No. 8. (Sep., 1993), pp. 523-532.

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Nest Predation and Nest Sites New perspectives on old patterns

Thomas E. Martin

I dentifying causes of general pat- terns of habitat selection, species coexistence, and life-history traits

are central issues in evolutionary ecol- ogy. Many organisms have been stud- ied to address these issues, but no group has had a greater influence on current perspectives than birds (Konishi et al. 1989).

Rapid advances came a few de- cades ago with work by Lack (1948, 1954), Hutchinson (1957,1959), and MacArthur (1958, 1972) and his as- sociates (Cody and Diamond 1975). These investigators argued that competition and food limitation were the major underlying influences of habitat selection, species coexistence, and life-history traits among birds (re- viewed in Martin 1986, 1987). In re- cent years, the ubiquity and impor- tance of competition and food limitation have been debated (Salt 1983, Wiens 1989).

Nonetheless, although the compe- tition paradigm has been challenged, alternative explanations are rarely explored for birds. New hypotheses need to be developed and examined, and they need to be directed at old and long-standing patterns that have been interpreted in the conventional per-

Thomas E. Martin is an associate profes- sor and assistant unit leader at the US Fish and Wildlife Service, Arkansas Co- operative Fish and Wildlife Research Unit, Department of Biological Sciences, Uni- versity of Arkansas, Fayetteville, AR 72701. His current address is the Mon- tana Cooperative Wildlife Research Unit, Department of Biological Sciences, Uni- versity of Montana, Missoula, M T 59812.

Nesting season can be a critical period for

maintenance of bird populations

spectives of competition and food limi- tation.

In this article, I focus on nest preda- tion as a process and nest sites as a resource. Predation is considered an important process in many systems (e.g., aquatic systems), but it has been neglected as an evolutionary process in avian systems (Martin 1988c, 1992b, Sih et a1 1985). This neglect of nest predation as an evolutionary force is surprising because population stud- ies indicate that nest predation is per- vasive; nest predation has been ob- served to be the primary source-of nest losses across a wide diversity of spe- cies, habitats, and geographic loca- tions, accounting for 80% of nest losses on average (Martin 1992a, 1993, Ricklefs 1969). Natural selec- tion should favor birds that choose habitats, communities, and life-his- tory traits that reduce the negative effects of nest predation given the importance of reproductive success to fitness. I will show how nest preda- tion and nest sites can provide viable alternative hypotheses for long-stand- ing patterns of habitat selection, spe- cies coexistence, and life-history traits that traditionally have been attrib- uted to food limitation and competi- tion.

Habitat selection and species coexistence More than three decades ago, MacArthur (1958) published a study, widely cited in general biology text- books, showing that five coexisting warbler species differed in their forag- ing locations and methods (Figure la). This partitioning of resources among coexisting species is an old and well- studied pattern that has long been considered necessary for coexistence (reviewed in Schoener 1974, 1986). MacArthur and others also showed

The colors of this female orange-crowned warbler, as it stands on the edge of a nest under a maple stem, are similar to the colors of the plants and litter surround- ing the nest site. Photos: Thomas E. Martin.

September 1 993

Birds are often inconspicuous in their nests in the sites they choose for nrs~1115. lhis female orange-crowned warbler (center of photo) has nested in a site without woody vegetation.

that numbers of coexisting bird spe- cies increase with vegetation density and spatial heterogeneity (Karr and Roth 1971, MacArthur et al. 1962, Willson 1974), a pattern that exists in many other animal foraging systems, including lizards, mammals, freshwa- ter fish, and marine intertidal organ- isms.

These two well-documented pat- terns generate two questions: Why is foliage density important to choice of habitats? Why do increasing numbers of species coexist in habitats with more foliage and greater structural heterogeneity? Historically, these questions have been explained in terms of food limitation and competition: birds were thought to choose habitats with greater foliage density because more foliage provided more food, and more species were thought to coexist in habitats with greater structural het- erogeneity because there were more types of foraging sites to partition to minimize competition (MacArthur 1958, 1972, MacArthur et al. 1962; see Martin 1986). Yet, evidence of competition and food limitation was indirect or absent, and other processes were not examined.

Habitat selection. Dense foliage and increased structural heterogeneity can affect habitat choice by reducing risk of predation in aquatic systems (e.g., Sihet al. 1985, Werner and Hall 1988). Birds may similarly choose habitats with dense vegetation to reduce the probability of nest predation. Foliage next to the nest can reduce the prob- ability of predation by concealing the nest. Indeed, predation rates were lower at nests with greater conceal- ment in 29 of 36 studies (Martin 1992a). At a larger spatial scale, foli- age in the patch (5-meter radius circle) surrounding the nest may also influ- ence predation risk; dense and com- plex vegetation may impede the abil- ity of mobile predators to locate sedentary prey (e.g., nests), even when the prey are poorly concealed. The latter result is expected primarily if predators are searching vegetation randomly. However, bird species (and sedentary organisms) usually special- ize on individual plant species for nesting and, thus, do not use vegeta- tion randomly. In such cases, preda- tors waste time and effort if vegeta- tion is searched randomly. Instead, predators should only search substrate

types that represent potential sites for encountering prey.

As a result, pfedation risk and patch choice may be influenced by numbers of potential prey sites rather than foliage density per se, thereby creat- ing two mechanistic hypotheses. The total-foliage hypothesis states that reda at ion risk decreases with increases in total vegetation in the nest patch because greater foliage density inhib- its transmission of visual, chemical, or auditory cues by prey. The poten- tial-prey-site hypothesis states that increases in the density of plants of the type used by prey reduces the prob- ability of predation because it increases the number of potential prey sites that must be searched and can cause the predator to give up before finding the occupied site.

I tested the response of predators to numbers of unoccupied and occupied sites using artificial nests baited with quail (Coturnix coturnix) eggs (Mar- tin 1988b). I put out seven nests per patch and varied the number of egg- containing nests in each patch (one, three, or seven of the seven nests con- tained eggs). Each of the three experi- mental treatments was represented by ten patches. Predation rates for any nest in a ~ a t c h decreased with in- creases in ;he number of nests that were unoccupied (Martin 1988b). Such results show that predators can re- spond to numbers of unoccupied and occupied prey sites, at least in an artificial setting.

Potential prey sites are represented in a natural setting by plants of the species and size used for nesting. Nest predation should decrease with in- creased number of these ~ l a n t s under one of the simplest situations of the potential-prey-site hypothesis. Under the total-foliage hypothesis, preda- tion should decrease with increases in numbers of total stems rather than the subset of stems of the type used for nesting. These predictions were tested on study sites in high-elevation snow- melt drainages in Arizona (Martin 1988a) by counting the number of stems in a 5-meter-radius circle sur- rounding nests. Analyses of hermit thrushes (Catharus guttatus) and MacGillivray's warblers (Oporomis tolmiei) support the potential-prey- site hypothesis; nest predation was reduced when the nest patch con- tained more potential nest sites (Fig-

BioScience Vol. 43 No. 8

ure 2). The total foliage hypothesis was rejected for both species; preda- tion rates were not reduced at nests surrounded by more total vegetation stems (Figure 2; also Martin and Roper 1988).

predation risk is not necessarily always high in small patches (few potential prey sites); if birds only used large patches, then predators should ignore small patches in the same way they ignore unused substrate types, and anv bird that used a small ~ a t c h would escape predation. Of course, predators would learn to explore small patches as numbers of prey using them increased. and vredation rates would quickly ekala& because of the low search time in small patches. This arms race should ultimatelv level off with birds using patches in proportion to their relative abundance and the amount of time it takes the predator to search them. Thus, some birds (con- specifics or a different species) should use small patches; in Arizona, green- tailed towhees (Pioilo chlorurus) choose small patchei of firs, whereaH hermit thrushes and MacGillivray7s warblers mostly choose large patches.

If birds select nesting patches that reduce predation risk, then they should choose patches with greater numbers of ~otential nest sites in situations in wgich these are the patches with the least risk of predation (e.g., hermit thrush and MacGillivray's warbler). Patches used for nestine were com- pared to unused patches :entered on a stem of the same type used for the nest (nonuse patches). These comparisons showed that patches used for nesting by MacGillivray7s warblers and her- mit thrushes did indeed have more potential prey sites, but not more total vegetation, than nonuse patches (Mar- tin and Roper 1988).' Such choices minimize predation risk given the pat- terns of predation found for these two species (i.e., Figure 2). Moreover, some species, such as the hermit thrush, do not forage in vegetation of the type used for nesting, so abundance of foraging sites can be eliminated as a basis for these nest patch choices (see Martin and Roper 1988). Thus, birds choose nest sites and patches with reduced risk of nest predation.

Predation risk can increase with prey density (Martin 1 9 8 8 ~ ) ~ but such

'T. E. Martin, 1993, unpublished data.

The colors of this female red-faced warbler, sitting on its nest, match some df the colors of the general area-even the orange color of the bird's face resembles the color of some leaf elements in the surrounding litter. The color and brightness of this site contrasts with that of the orange-crowned warbler (see photo page 523).

effects could be offset by greater num- standing relationship between bird bers of potential prey sites, given that species numbers and foliage profiles. the latter apparently reduce predation Of course, such effects do not elimi- risk. Consequently, numbers of indi- nate the possibility that food limita- viduals and species may increase with tion and competition are also operat- foliage density due to increasing num- ing, but the results challenge the bers of potential nest sites (Martin priority of the latter processes and 1988a), rather than the historical ar- show that they certainly are not the gument of greater .numbers of forag- only explanations for these patterns. ing sites (e.g., MacArthur 1972, MacArthur et al. 1962). Coexistence of species. Nest preda-

I tested this possibility by re- tion may also affect the types of spe- analyzing a classic study by Willson cies that successfully coexist, based (1974); she showed that bird species on similarity of their nest sites. When numbers increased with the addition different species use the same site for of shrub and tree layers, but she ques- nesting, then density of potential prey tioned the importance of foraging sub- sites is held constant but prey density strates to this result. I reanalyzed her for that site is increased by coexist- data by classifying species based on ence (Figure 3b). If predation risk nesting versus foraging sites and found increases with cumulative prey den- that more of the species that were sity, then predation risk should in- added with shrub and tree foliage crease for all species using similar nest layers were species that nested in those sites and thus exert negative selection layers than species that foraged in on coexistence (Martin 1988c; also them (Martin 1988a). Moreover, ex- see Holt 1977,1984). If these species amination of the correlation between use different nesting sites, then the number of species and density of foli- predator must search more substrates, age in these above-ground layers thereby reducing search efficiency and showed that almost 20% more of the reducing the cost of coexistence (Fig- variation in species numbers was ex- ure 3a). When nest site differences are plained based on nesting preferences sufficiently large to make searching than on foraging preferences. both sites too costly to the predator,

Similar results were obtained for then coexistence should not affect my sites in Arizona (Martin 1988a). predation rates. Such effects can favor Thus, availability of nest sites with coexistence of species that use differ- low risk of predation provides a strong ent nest sites (Martin 1988b,c). These alternative explanation for the long- nest site differences can occur in two

September 1993

A red squirrel (Tamiasciurus hudsonicus) robs a bird nest. This photo was taken by an automated camera.

spatial dimensions: vertical (i.e., among vegetation layers) and hori- zontal (i.e., among substrates or mi- crohabitats in the same vegetation layer).

I used artificial nests to experimen- tally test the prediction that predation favors nest site differences among co- existing species (Martin 1988 b). Nests were placed in positions that simu- lated nesting locations of four species occurring on the study sites in Ari- zona. Nests were divided among the sites of these four species in one treat- ment to simulate coexistence of four species that use different nest sites (Figure 3a). In a second treatment, nests were placed at the same total density but were placed in only one of the four sites to simulate all four spe- cies using the same site (Figure 3b). Predation rates were ~redicted to in- crease when cumulative density of nests increased in a particular nest site due to overlapping use by coexisting species (Martin 1988~). Indeed, nest predation rates were much greater when the simulated species used the same site than when they used differ- ent nest sites (Figure 4). Thus, these experiments indicate that nest preda- tors exhibit behaviors that can favor nest site differences among coexisting species.

Examination of nest site use by birds on my Arizona sites indicated that they do in fact differ in where they place their nests in vertical and

horizontal nesting space. The 12 spe- cies on the Arizona sites were dis- persed vertically, with four species nesting on the ground, three species nesting in the shrub layer, two species nesting in the subcanopy, and three species in the ~ a n o p y . ~ Data from other avian communities also showed that birds were, moreover, dispersed vertically based on their nesting sites than on their foraging sites (Martin 1988~) .

species within a vegetation layer differed in nest substrates and micro- habitats along a short moisture gradi- ent in the Arizona snow-melt drain- ages (Figure lb). Each of the four ground-nesting species places nests at the base of different plant species (Fig- ure 5) that occur at different abun- dances along the moisture gradient (Figure lb). The three shrub-nesting species overlap in substrate use (all use small firs), but they chose these firs in different microhabitats along the moisture gradient; green-tailed towhees chose small firs in drier sites where New Mexican locust was more abundant. whereas MacGillivrav's warblers chose small firs in patc6es with more maple, and hermit thrushes chose small firs in patches with more small firs than the other two specie^.^ These differences in nest site use among coexisting species are greater than for foraging sites because birds specialize (use a site more than 60% of the time) on nest sites that differ among species (e.g., Figure 5), whereas birds are much less specialized and overlap more based on foraging sites (Figure la).

If nest predation favors this use of different nest sites by coexisting spe- cies (or favors coexistence of species that already use different sites based on their evolutionary histories), pre- dation rates should be greater for spe- cies that use nest sites that are similar to those used by other species. Indeed, predation rates were greater for guilds (shrub nesters) and species within a guild that placed a greater proportion of their nests in sites that were similar to other coexisting species.'

The cost of using nest sites that are similar to other coexisting species is clearly shown by MacGillivray's war- blers. They place their nests in small

=See footnote 1. 'See footnote 1. 'See footnote 1.

firs or short maple thickets. Small firs are also used as nest sites bv hermit thrushes and green-tailed {owhees, whereas MacGillivray's warbler is the only species that uses the short maple thickets on these sites. As a result, cumulative nest density in small firs is slightly more than four times as great as in the maple. If predators respond to cumulative densities, predation rates should be greater for Mac- Gillivrav's warblers nests in small firs than thbse in maple. ~ndeed, daily mortality rates were significantly greater in firs than in maple (Figure 6), and total percentage of nests lost to predation was substantially greater in firs (78.3%) than in maple (39.0%). Moreover, experiments with artificial nests showed that this trend could be reversed by increasing the cumulative density of nests in maple compared with small firs: when nests in m a ~ l e were four times as dense as nests in small firs, daily mortality rates of nests in maple were much higher than for nests in small firs (compare striped bar of maple with open bar of fir in Figure 4). Such results show that dif- ferences in reda at ion rates between these substrites are from differences in density of nests rather than differ- ences in the substrates.

In summary, artificial and real nests show that risk of nest predation in- creases with overlap in nest site use among coexisting species and thereby provides a strong alternative hypoth- esis to food-based competition for resource partitioning among coexist- ing species. Indeed, partitioning of microhabitats among coexisting spe- cies is much greater when based on nest sites (Figures 1 b and 5) than on foraging sites (Figure 1 a). Moreover, the results show a direct fitness cost (i.e., increased nest predation) with overlap in nest site use among coexist- ing species, whereas fitness costs of overlap in foraging sites are largely undocumented.

Constraints of evolved nest placement on local success Predation may favor nest site special- ization within species because use of new sites may either overlap sites al- ready used by other coexisting species or because species may not be adapted to new sites in terms of, for example, cryptic coloration or physiological

BioScience Vol. 43 No. 8

Cape May Blackburnian Black-throated Bay-breasted Myrtle warbler warbler warbler green warbler warbler

,Green-tailed towhee Giilivray's warbler

Hermit thrush

Figure 1. a. Foraging locations of five species of warblers coexisting in northeastern spruce woods (modified from MacArthur 1958). The diagram indicates six vertical and three horizontal zones in trees that are most frequently used by each warbler species. The zones of most concentrated activity are shaded such that at least 60% of the observed foraging attempts are in the shaded zones (MacArthur only shaded to 50% in his original article). Numbers are the percentage of observed foraging attempts in shaded zones. Note that any zone of concentrated activity in the top three vertical layers (only the myrtle warbler uses lower zones) is usually used as a zone of concentrated activity by at least three species. In fact, the cumulative percentage of time spent in any zone by all species combined is greater than for any individual species that concentrates activity in that zone. In short, species overlap markedly in their use of any foraging zone even when only considering the zones that comprise 60% of the foraging activity. b. Schematic drawing of vegetation and bird distribution along a moisture gradient in snow-melt drainages in Arizona (unpublished data). The lower parts of drainages are moist and characterized by plant species such as canyon maple (Acer grandidentatum) and quaking aspen (Populus tremoloides). The upper sides of drainages are drier and typified by xeric-tolerant plant species such as New Mexican locust (Robinia neomexicana). Small white firs lAbies concolor) were distributed throighout the entire gradient. These gradieAts (i.e., hillsides) are generally only 35-70 m in length. The four ground-nesting bird species (identified underneath the gradient) nest at the base of different plant species that occur at different points along the gradients. When the plant species that comprise 60% of the nest substrates for a species are examined, almost no overlap in nest substrate use occurs among species (see Figure 5) . The three shrub-nesting bird species (identified above the gradient) all use small firs but use the firs in different parts of the gradient such that the microhabitat conditions surrounding the firs differ.

tolerance to the microclimatic condi- strate type; e.g., Figure 5 ) .Moreover, tions. Indeed, data from Arizona show a review of the literature also revealed nest predation is greater in less fre- that most species are specialized in quently used nest sites,j and most This special- their nesting ~ u b s t r a t e . ~ species were substrate specialists ization contrasts with foraging sites (more than 60% of nests in one sub- where species are much less special-

'See footnote 1. 6T.E. Martin, 1993,manuscript in preparation.

September 1993

ized and overlap more (Figure l a ) . Specialization may also lead to ste-

reotypy in nest placement. Nest heights of 1 7 warbler species were compared over latitudes differing by as much as 14", and only 4 species shifted heights significantly despi te geographic changes in vegetation structure and types of coexisting species (Martin 1 9 8 8 ~ ) .Moreover, in many cases, all or most bird species within a genus use the same vegetation layer or gen- eral substrate type for nesting. Such results suggest that nest placement often is evolutionarily conservative.

Nest placement may be set for a species over a large geographic area based on events during speciation or their evolutionary history. Stereotypy in nest placement could result in poor re~roductivesuccess in some habitats and even select against occupation of those habitats, potentially providing a mechanism for favoring coexistence of species that differ in nest place- ment. For example, hermit thrushes are subject to more intense predation than any other species on my study sites in Arizona. This intensity of pre- dation is closely related to the use of small firs for nesting.

Given that nestinr! is so unsuccess- ful in small firs, i h y choose such sites? Hermit thrushes may be immi- grating t o my sites from other sites where small firs are an appropriate choice for nesting. Firs may elicit a settling response when encountered by dispersing birds, because firs are an appropriate proximate cue over the larger range of the population. In- deed. the race of hermit thrush that occurs on my sites usually uses small conifers for nesting throughout its western range (Harrison 1979). Such sites may be appropriate over most of the range, but inappropriate on my study areas.

My study sites are drainages that are located within 8 km of the edge of the Mogollon Rim, an abrupt cliff that represents the southern extension of the Colorado Plateau. The edge of the rim has a narrow band of moist vegetation (e.g., maple) associated with greater precipitation formed by the u ~ w a r d deflection of air at the rim face. My study sites are in this narrow band of moist vegetation. Red squir- rel distribution and densities are asso- ciated with maple on these sites (Up- hoff 1990). Photos from automated

527

- -- -- - --

--

0.10- Ma&~ll~vrays warbler

0.00..

0.06.-

0.04.-0)C

0.02-

2.-1SE

0.00-

o m - Herrntt thrush %.-

0.05

-.--Few Many Few Many

Potential Total stems nest sites

Figure 2. Daily mortality rate (rate at which nests are lost to predators per day) and its standard error for nests in patches with less (few) or more (many) than the median number of stems that represent potential nest sites or total vegetation (total stems). Z-values were calculated using the z-test of Hensler and Nichols (1981). For the MacGillivray's warbler, 62 nests were observed. For potential nest sites, z = 2.5 (p = 0.006); for total stems, z = 0.9 (p = 0.19). For the hermit thrush, 109 nests were observed. For potential nest sites, z = 2.5, p = 0.006; for total stems, z < 0, p > 0.5.

cameras at artificial nests showed that red squirrels are the major predators on nests and account for more than 80% of nest predation events (Martin 1988b).'Moreover, these maple habi- tats contain MacGillivray's warblers and green-tailed towhees, both of which use small firs as nest sites and thereby overlap hermit thrushes and increase the cumulative density of nests in firs.

If the low nesting success of hermit thrushes in maple drainages is due to the high density of red squirrels and high cumulative density of nests in small firs, then nesting success should be higher in the same nest sites (small firs) in other habitat conditions with- out coexisting species. Indeed, success of hermit thrush nests in small firs in nearby drainages that do not contain maple or the other two coexisting species was markedly higher than in maple drainages (Figure 7).

'See footnote 1.

528

MacGillivray's warbler poses a similar problem: Given that nesting success is so much greater in maple thickets (Figure 6), why use firs? MacGillivray's warbler usually places only approximately one third of nests in small firs (Table 1).This use of conifers again reflects a common pat- tern throughout their range.s How- ever, small firs may be used when short maple thickets are not available. Many of the territories where small firs are used have less short maple.9

Western Foundation of Vertebrate Zoology, 1993, Los hngeles, C h , unpublished data. ySee footnote 1.

Case a

Case b

Moreover, annual differences in nest sites also suggest that availability is important. In the four years before 1988 and 1989, maples were used for approximately two thirds of the nests. In 1988 and 1989, late freezes and a drought, respectively, inhibited leaf development in maples, and Mac- Gillivray's warblers placed two thirds of their nests in small firs (Table 1 ) . The increased use of small firs by MacGillivray's warblers in 1988 and 1989 was associated with significantly greater nest predation in these two years compared with the four previ- ous years. Moreover, predation rates were correlated with the proportion

Figure 3. Schematic drawing of substrate and prey distribution for two experimental nest treatments. In both cases, four types of nest sites are represented by four open symbols. Four bird species are represented by four solid symbols. In the first treatment (case a), each species occupies a different nest site. In the second treatment (case b), density is the same as in case a, but all species occupy the same nest site. The result is that cumulative density in a nest site (e.g., circles) is four times greater when species use the same nest site (case b) than when each species uses a different nest site (case a). Note that almost all circles are occupied in case b, rewarding predators to continue searching the substrate type but to ignore other substrate types because they are empty. This situation increases predation rates on all species using the substrate type. In contrast, in case a, the predator must search all substrates to encounter the same number of prey, and the increased encounters with unoccupied sites may cause the predator to give up before finding a prey, thereby reducing the cost of coexistence.

BioScience Vol. 43 No. 8

Ground Maple Fir Maple (1m) (3m)

Nest position

Figure 4. Mean (and standard error) in daily mortality rates (rate at which nests are lost to predators per day) for artificial nests when nests were placed among four different types of sites (open bars, case a of Figure 3) and when nests were all placed in the same type of sites (striped bars, case b of Figure 3). Density of nests was held constant between the two treat- ments. A total of 480 nests were used among three replicate sites and over two temporal replicates. The situation of nests placed in the same type of sites was not tested for the 3-meter maple. Data from Martin (1988b).

of nests placed in small firs by MacGillivray's warblers among years. Thus, availability of suitable nest sites apparently can influence the success of a population within a habitat by influencing predation risk.

In summary, nest predation repre- sents a potentially strong selection pressure and forms a viable alterna- tive hypothesis to food limitation and competition for general patterns such as the increase in numbers of species with foliage density and dispersion, differences in microhabitat use among coexisting species, and differences in nesting success of populations among habitats. The role of nest predation as

Orange-crowned warbler

Q) 0Virginia's warbler v,2 C 0 %

E 0.5 Q)3 u2 U.

0.0 Firs Maple

an influence on nest-site selection may also indirectly affect other traits (e.g., life-history traits) that are affected by nest sites (Martin 1988d).

Life-history traits Life-history studies represent one area in which nest reda at ion has not been totally ignored. Yet, food limitation is still thought to be the most important influence on life-history traits (Lack 1948, 1954, reviews in Martin 1987, 1992b) and, ironically, the most widely touted example of nest predation ef- fects (large clutch size of cavity-nest- ing birds) may be incorrect. The large clutch sizes of cavity-nesting birds compared with open-nesting birds have long been considered a conse-

u

quence of reduced nest predation on cavity nesters (Lack 1948,1954, Lima 1987, Slagsvold 1982). Nest preda- tion is indeed generally less for cavity- nesting than open-nesting birds (Mar- tin and Li 1992; but see Nilsson 1986), but nest ~ r eda t i on has not been di- rectly testkd as the cause of the clutch size pattern. Here, I examine nest predation and two other hypotheses.

Recent inters~ecific analvses dem- onstrate that adult survival varies in- versely with fecundity in both Europe (Bennett and Harvey 1988, Szther 1988) and North America (Martin in press a) . This inverse relationship may occur because fecundity derives from adult mortality (e.g., Law 1979) , which allows one hypothesis for the clutch size differences between cav-ity-nesting and open-nesting birds. The winter mortality hypothesis states that a greater proportion of cavity nesters

Red-faced warbler

Dark-eyed junco

Locust Open Nesting substrate

Figure 5. Frequency that ground nests were placed below the indicated plant species by the four ground-nesting species. Orange-crowned warbler (Vermivora celata; n = 90; black bars), Virginia's warbler (Vermivora virginiae; n = 27; open bars), red-faced warbler (Cardellina rubrifrons; n = 30; shaded bar), and dark-eyed junco (Junco hyemalis; n = 55; cross-hatched bar).

September 1993

Table 1. Annual variation in nest preda- tion as a function of variation in use of nesting substrates by MacGillivray's war- blers. The increased use of firs in 1988 and 1989 was associated with signifi-cantly greater nest predation than in the previous four years (X2 = 6.95, p = 0.008, multiple comparison test of Sauer and Williams 1989).Predation rates were correlated with proportion of nests built in firs (r = 0.89, p < 0.05).

Percentage of Percentage of nests built in nests lost to

Year predation Firs Maple

1984 55 0.33 0.67

than open nesters are residents, and winter mortality is thought to be greater for residents than migrants (Greenberg 1980, von Haartman 1957,1968). Thus, larger clutch sizes of cavity nesters may be a byproduct of greater adult mortality caused by residency habits.

Reproductive traits may not derive from adult survival, however. Instead, adult survival may derive from differ- ences in reproductive output (Charnov and Krebs 1974, Williams 1966), af- fecting two hypotheses. The nest pre- dation hypothesis states that reduced nest predation is thought t o allow more young to be fed over a longer nestling period (Lack 1948, 1954) or more energy to be invested in a single nesting attempt rather than several (e.g., Slagsvold 1982). As a result, reduced nest predation is thought to favor larger clutch size (Lack 1948, 1954, Law 1979, Lima 1987, Slagsvold 1982), which should cause decreased or no change in adult survival. The limited breeding opportunities hypoth- esis states that when breeding oppor- tunities are limited, birds should in- vest increased effort in reproduction (i.e., large clutch size) at the cost of reduced survival when they get a chance to breed because they may not get another chance (Martin 1992b, in press b). Hence, cavity nesters whose breeding opportunities are limited by availability of nest holes should have larger clutch sizes, causing lower sur- vival, than open-nesting birds.

Greenberg (1980) concluded that residents suffered higher adult mor- tality than migrants (represented by

529

Fir Maple

Nest substrate type

Figure 6 . Daily mortality rates (and stan- dard errors) for nests of MacGillivray's warblers in small white firs and canyon maple. Daily mortality rates were much greater ( z = 2.85, p = 0.0022) for nests in firs than for nests in maple. There were 30 nests in firs and 32 nests in maple.

the combined data in Figure 8). How-ever, he confounded migrant classifi- cation and nest type. I reanalyzed the data and separated nest type from migration habits. Analysis of variance showed that adult survival did not differ between migrants and residents within a nest type (i.e., open nesters; Figure 8). On the other hand, survival differed between nest types (open nest- ers versus cavity nesters) within resi- dents.

The same results are obtained when based on a larger data set with even finer division in migration habits (Fig- ure 9); survival does not differ among migration classifications within a nest type, but it does differ between nest types within a migration classifica- tion when body mass effects are con- trolled through two-factor analysis of covariance.

The similar adult survival of resi- dents and migrants when nest type is controlled (i.e., within open nesters and nonexcavators) falsifies the win- ter-mortality hypothesis, which pre- dicts that residents suffer greater adult mortality than migrants. Moreover, not all resident cavitv nesters suffer greater adult mortality than open nest- ers; resident cavity-nesting species that excavate their own nest holes (exca- vators) have adult survival rates that are greater (0.65 2 .028 [standard error], n = 5 ) than for either resident nonexcavators (species that do not excavate but instead use existing holes) or resident open nesters (Figure 9 ) with body mass controlled (ANCOVA, F = 12.73, p < 0.0001).

The evidence also favors rejection of the nest-predation hypothesis. Nest

mortality predictably averages much less for excavators (13% of nests are lost) than nonexcavators (36% loss; Martin and Li 1992). Yet, excavators have smaller clutches (Martin and Li 1992) and greater adult survival (Fig- ure 9) than nonexcavators, counter to the nest-predation hypothesis, which predicts that excavators with reduced nest predation should have larger clutch size and lower or similar adult survival compared wi th nonex-cavators. Moreover, analysis of life- history traits for 110 species of North American birds shows that clutch sizes of nonexcavators are outliers for their nest predation rates (Martin in press a). Such results indicate that the large " clutch sizes of nonexcavating cavity nesters cannot be explained by the nest predation hypothesis. Plus, the patterns are not explained by phylo- genetic effects (Martin in press b, Martin and Li 1992).

The data are consistent with the limited-breeding-opportunities hy- pothesis. Nest sites are much more limited for cavity-nesting birds that

Maple Maple Nonmaple (All years) (1989, 1991) (1989, 1991)

Drainage type

Figure 7. Nesting success of hermit thrushes in maple drainages pooled across eight years (1984-1991) and in two years (1989, 1991) when both maple and nonmaple drainages were studied. Maple drainages are the snow-melt drainages that have been the focus of my studies in Arizona. Nonmaple drainages are nearby drainages that have small firs but do not contain maple. Total nesting success (per- centage of nests that fledge at least one young) was 8.0% (out of 195 nests) for maple drainages in 1984-1991; 8.7% (out of 103 nests) for maple drainages in 1989 and 1991; and 38.9% (out of 17 nests) for nonmaple drainages in 1989 and 1991. The success of nests in nonmaples drainages was markedly higher than in maple drainages either in the same study years (X2 = 10.9, p = 0.001) or compared to nest success pooled across years (X2 = 15.2, p = 0.0001).

,,,

75,

0.55

2 - o.,5

4 a

0.35

Combined Open Cavity

Nest type

Figure 8. Annual adult survival for resi- dent (open bars) versus migrant birds (shaded bars) when nest type is combined or separated. Data are from Greenberg (1980). Numbers in parentheses repre- sent numbers of species. Midpoints were used for data presented with ranges. Cav- ity nesters include only species that do not excavate their own cavities. Data for blue tit (Parus caeruleus) on Canary Is- land were excluded because island DODU-

L L

lations are known to exhibit higher sur- vival than mainland populations. Data for brown-headed cowbird (Molothrus ater) also were excluded because this species lays its eggs in the nests of other species. Analysis of variance showed that adult survival did not differ (F = 0.98, p > 0.10) between migrants and residents within a nest type (i.e., open nesters). On the other hand, survival differed (F = 13.14, p = 0.002) between nest types (open nesters versus cavity nesters) within residents.an influence on nest-site selec- tion may also indirectly affect other traits (e.g., life-history traits) that are affected by nest sites (Martin 1988d).

depend on finding an existing hole (nonexcavators) than for open nesters (Martin and Li 1992, von Haartman 1957,1968), and nonexcavators have larger clutches and lower adult sur- vival than open nesters, as predicted by the limited-breeding-opportunities hypothesis. In addition, nest sites are also more limited for nonexcavators than excavators, because excavators can create their own cavities (Wes- olowski 1983) andnonexcavators have larger clutches and lower adult sur- vival than excavators, again as pre- dicted by the hypothesis. Thus, com- par i son of adu l t mor ta l i ty for nonexcavators versus both open nest- ers and excavators supports the lim- ited-breeding-opportunities hypoth-esis and rejects the two alternative hypotheses.

Excavators as a group provide ad- ditional support for the hypothesis. Excavators vary in their abilities to excavate holes because of morpho-

BioScience Vol. 43 No. 8 530

logical differences, and species with weaker excavating morphology de- pend on existing holes more; such species potentially are more limited in their nesting opportunities, and clutch sizes increase with this dependence on existing holes as expected under the limited-breeding-opportunities hy-pothesis (Martin in press b). More- over, excavators that use old holes apparently suffer greater nest preda- tion (Nilsson et al. 1989 j, and, hence, the larger clutch sizes of these species is further evidence against the tradi- tional nest predation hypothesis. Pre- dation may contribute to clutch size differences indirectly by influencing nest site preferences, nest size, or num- ber of broods (Lima 1987, Martin 1988d, in press a, Martin and Li 1992, Moller 1987, 1989, Slagsvold 1982). However, nest site attributes appar- ently are more important to differ- ences in clutch size and adult survival among cavity-nesting bird species than are differences in nest predation or food limitation (Martin and Li 1992, Martin in Dress bj.

These risults emphasize the impor- tance of examining new hypotheses rather than blindly accepting long- standing dogmas. Indeed, although nest predation appears to be less im- portant to life histories of cavity-nest- ing birds, nest predation apparently influences life-history traits among many groups of birds for which food limitation traditionally has been con- sidered to be more important (Kulesza 1990, Martin 1993, in press a).

Conservation implications The pervasive nature of nest preda- tion and the influence of nest sites on oredation risk indicates that nest sites are important habitat components and that the nesting season can be a criti- cal veriod for maintenance of bird populations. Conservation of species depends on knowing their breeding biology and identifying and preserv- ing the habitat features that affect

u

breeding productivity and survival (Martin 1992a). Yet, insufficient in- formation is available for most sue- cies with regard to their habitat neehs, reproduction, and survival.

Nest predation has gained consid- erable attention in conservation stud- ies because nest predation can in-crease with fragmentation (e.g.,

September 1993

All estimation methods

O.=T

2 V)- ,,mesf Jolly-Seber methods

Residents SD LD migrants migrants

Figure 9. Annual survival rate for North American bird species separated by mi- gration habits and nest type (open nests, open bars; cavity nests, shaded bars). Numbers in parentheses are numbers of species. Data are from Martin and Li (1991). Cavity nesters include only nonexcavators. Four methods of estimat- ing adult survival, all based on recapture1 recovery, were used by the studies. The Jolly-Seber method is the most rigorous estimation method; it is separated to test any potential bias due to differences In estimation methods. The patterns for the Jolly-Seber estimates are identical to the patterns for all methods combined. Sur- vival does not differ among migration classifications within a nest type (F = 0.72, p > 0.10) but does differ between nest types within a migration classifica- tion (F = 15.32, p c 0,0001) when body mass effects are controlled through two- factor analysis of covariance.

Wilcove 1985) and potentially cause loss of species (local extinction) from fragments. Such effects have been con- sidered primarily in terms of the in- crease in predators along edges of habitat fragments (Wilcove 1985 and many others). Yet, nest predation can- not fully explain losses of species from fragments (see Martin 1992a), and some assumptions regarding vulner- ability of species to nest predation are incorrect (Martin 1993 j.

Other ecological requirements of species are undoubtedly important to their loss. For example, the arguments and evidence presented here suggest that species commonly differ in their

nest site preferences, and these prefer- ences may be fixed. Habitat frag- mentation can cause direct loss of habitat features needed by some spe- cies and thereby cause loss of those species (Martin 1992a).

Even in large forest tracts without edge problems, alteration of condi- tions by grazing, lumber production, or other anthropogenic activities can potentially cause loss of necessary habitat conditions for some species. Moreover, habitat degradation may reduce the diversity of nesting sites available and cause increased preda- tion on species that still use such habi- tats because they are forced to use similar (overlapping) nest sites and increase cumulative nest density, or because species are forced to use poor- quality nest sites.

Such effects added to increased pre- dation along edges (Wilcove 1985) may cause many populations to re- produce well below levels necessary for maintaining populations. Indeed, a number of bird species are showing alarming population declines (Robbins et al. 1989). Correction of such popu- lation problems will depend on deter- mining the habitat features that allow successful reproduction by a variety of species on their breeding grounds, as well as habitats needed for survival on the wintering grounds. Given the importance of nest predation and nest sites to nest success, much greater attention is needed for these issues,

Acknowledgments I appreciate comments and thoughts on this manuscript by E. Bokman, W. Etges, S. Foster, S. Garner, R. L. Hutto, M. Newton, L. Petit, and anonymous reviewers. I thank a large number of field assistants for help in finding and monitoring nests. I thank the Blue Ridge Ranger Station of the US Forest Service for their support and permis- sion to work on their forest. My work has been supported by grants from the National Science Foundation (BSR- 8614598 and BSR-906320).

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Nest Predation and Nest SitesThomas E. MartinBioScience, Vol. 43, No. 8. (Sep., 1993), pp. 523-532.Stable URL:

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