Studies in Avian Biology No. 32:130–139

TROPHIC ADAPTATIONS IN SPARROWS AND OTHER VERTEBRATES OF TIDAL MARSHES

J. LETITIA GRENIER AND RUSSELL GREENBERG

Abstract. Tidal marshes present trophic challenges to terrestrial vertebrates in terms of both the abiotic (tidal fl ow and salinity) and biotic (vegetative structure and food resources) environments. Although primary productivity is high in tidal marshes, supporting an abundance of terrestrial and intertidal invertebrates, seeds, and fruit are far less abundant than in comparable interior habitats. In response to these food resources, terrestrial vertebrates in tidal marshes tend to be either herbivores or preda- tors on invertebrates, including marine taxa. We examine the trophic adaptations of sparrows in the subfamily Emberizinae, the vertebrate group that shows the greatest amount of divergence associated with colonizing tidal marshes. Across several different evolutionary clades, tidal-marsh sparrows tend to be heavier and have signifi cantly longer and narrower bills than their closest non-tidal- marsh relatives. The morphological divergence is greatest in taxa with longer associations with tidal marshes. We hypothesize that longer, narrower bills are an adaptation to greater year-round feeding on invertebrates, particularly benthic marine invertebrates, and a reduced dependence upon seeds. Tidal-marsh sparrows and a number of other terrestrial vertebrates share an additional indirect adap- tation to foraging in tidal marshes. Most specialized taxa exhibit grayer and blacker dorsal coloration (particularly in brackish upper estuaries) than their closest non-tidal-marsh relatives. We propose that this consistent shift in dorsal coloration provides camoufl age to terrestrial vertebrates foraging on exposed tidal sediments, which tend to be grayish to blackish in color due to the prevalence of iron sulfi des, rather than the iron oxides common to more aerobic sediments in interior habitats.

Key Words: bill morphology, biogeographic rule, ecological speciation, tidal marsh, trophic adaptation.

ADAPTACIONES TROFICAS EN GORRIONES Y EN OTROS VERTEBRADOS DE MARISMAS DE MAREA Resumen. Los marismas de marea presentan retos trófi cos para vertebrados terrestres en términos ambientales, tanto abióticos (fl ujo de la marea y salinidad) y bióticos (estructura vegetativa y recur- sos alimenticios). A pesar de que la productividad primaria es alta en marismas de marea, soportar una abundancia de invertebrados terrestres e intermareales, semillas, y frutas son mucho menos abundantes que en habitats interiores comparables. En respuesta a estos recursos de alimento, ver- tebrados terrestres en marismas de marea tienden a ser ya sea herbívoros, o depredadores de inver- tebrados, incluida taxa marina. Examinamos las adaptaciones trófi cas de gorriones en la subfamilia Emberizinae, el grupo vertebrado que muestra la mayor cantidad de divergencia asociada con la colo- nización de marismas de marea. A través de varias clades diferentes evolucionadas, los gorriones de marisma de marea tienden a ser mas fuertes y tienen signifi cativamente picos mas largos y mas delga- dos, que sus parientes mas cercanos de marismas que no son de marea. La diferencia morfológica es mayor en taxa con asociaciones más amplias con marismas de marea. Hacemos una hipótesis de que picos más largos y más delgados son una adaptación a una alimentación de invertebrados durante todo el año, particularmente invertebrados bénticos marinos, y una dependencia reducida a semillas. Los gorriones de marisma de marea y un número más de otros vertebrados terrestres comparten una adaptación adicional indirecta al forrajeo de marismas de marea. La mayoría de la taxa especializada, exhibe una coloración dorsal más grisácea y negra (principalmente en estuarios salobres más altos) que sus parientes más cercanos que no son de marismas de marea. Proponemos que este consistente cambio en la coloración en el dorso, provee camufl aje a los vertebrados terrestres que forrajean en sedimentos expuestos por la marea, los cuales tienden a ser grisáceos a negros de color, debido a la prevalecencia de sulfuros de hierro, en lugar de óxidos de hierro, comunes en sedimentos mas aeróbi- cos en habitats del interior.

Tidal marshes present profound adaptive habitats by elevation, creating a gradient of fl o- challenges to terrestrial vertebrates that attempt ristically distinct zones (Eleuterius 1990, Faber to colonize them. The physical infl uence of tidal 1996). At the lowest elevation, unvegetated tidal cycles and the chemical infl uence of salinity sloughs with periodically exposed mud offer combine to create a wetland ecosystem where another habitat absent from other wetlands. the benthic environment has strong marine char- Although tidal marshes can be quite produc- acteristics, yet the vegetative layers resemble tive, providing ample trophic opportunities to freshwater marsh habitats (Chabreck 1988). The support dense vertebrate populations, these frequency of tidal inundation varies across marsh marshes are generally quite restricted in the 130 TROPHIC ADAPTATIONS—Grenier and Greenberg 131 area they cover relative to interior habitats and tidal-marsh populations were allopatric (Chapman 1977). Therefore, the population at the time of marsh colonization, directional size of a terrestrial vertebrate inhabiting a tidal selection may cause rapid divergence of the marsh is likely to be small compared to popula- marsh populations. Possible examples of tion size in upland habitats. Finally, most tidal taxa that underwent speciation following dif- marshes formed well after the receding of the ferentiation resulting from adaptation to the ice during the last glaciation and, thus, were marsh environment are the Clapper Rail (Rallus colonized by upland species over a relatively longirostrus), Seaside Sparrow (Ammodramus short span of time from an evolutionary per- maritimus), the Saltmarsh Sharp-tailed Sparrow spective (Malamud-Roam et al., this volume). (Ammodramus caudacutus), the salt marsh har- The infl uence of glaciation probably means that vest mouse (Reithrodontomys raviventris), and tidal-marsh taxa suffer from repeated episodes the salt marsh snake (Nerodia clarkii). of local extinction or signifi cant population After a certain point, specialization for tidal bottlenecks. marshes might hinder competitive ability in the The abundant food resources and sharp envi- habitat of origin, thus further reducing the pos- ronmental gradient between marsh and upland sibility of gene fl ow and favoring the local adap- favor local adaptation of tidal-marsh taxa, while tation to tidal-marsh conditions. Eventually, the ephemeral nature of tidal-marsh habitats extreme specialization for saltmarshes might and their geographically restricted distribution reduce competitive ability even in brackish inhibit differentiation. Thus, the empirical ques- marshes, allowing a second wave of invasions tion remains: How much adaptive differentia- in brackish marshes by upland colonists. tion characterizes tidal-marsh vertebrates, and how do these adaptations develop? THE COMPARATIVE APPROACH TO THE STUDY OF TIDAL-MARSH ADAPTATIONS PROPOSED TAXON CYCLE FOR TIDAL- MARSH VERTEBRATES A time-honored approach to studying adap- tation is examining patterns of phenotypic Trophic adaptation to tidal-marsh resources variation among unrelated taxa across a similar probably occurs in several stages, paralleling environmental gradient. The approach of relat- taxon cycles proposed for the evolution of biota ing geographic variation to causal explanations in other systems (Ricklefs and Bermingham of adaptation in vertebrates has led to the devel- 2002). First, as estuaries form and tidal-marsh opment of a number of biogeographic rules that vegetation develops; animals that can with- are both useful and controversial (Zink and stand the physical challenges colonize the Remsen 1986). emerging marsh to take advantage of abundant Differentiation of tidal-marsh taxa is food and few competitors. Second, the lack of prevalent in vertebrates along the Pacifi c and competitors in tidal marshes allows for niche Atlantic coasts of North America, particularly expansion and ensuing increased variation in among sparrows of the subfamily Emberizinae. trophic-related characters (e.g., diet, bill, legs, Ten sparrow species or well-marked subspe- and feet). Third, if gene fl ow is reduced between cies have been described as endemic to tidal tidal-marsh and non-tidal-marsh conspecifi cs, marshes. Because emberizids have colonized selection would drive adaptation to the novel tidal marshes at various times and along dif- tidal-marsh conditions. Initial diversifi cation ferent coastlines, we focus mainly on the (from step 2) would provide the genetic vari- trophic adaptations of this particular group ance for selection to act upon. Gene fl ow is of vertebrates. However, we discuss other ter- likely to be reduced in situations where tidal- restrial-vertebrate taxa when comparisons are marsh populations are geographically isolated. appropriate. Where populations are parapatric, assortative The mere correlation between geographic mating by habitat, which is easy to invoke for variation and occupancy of a particular habitat territorial passerines, may allow speciation to does not prove that tidal-marsh populations occur even in the face of relatively high levels of are responding adaptively to a selective gra- gene fl ow (Rice and Hostert 1993). In this case, dient associated with that habitat. In order to diversifying selection for effi cient exploitation use this comparative approach to develop an of tidal marshes and upland foods may create adaptive hypothesis for a particular character, resource polymorphisms in trophic-related we look for the following lines of evidence: (1) characters (Skulason and Smith 1995). These A similar pattern of phenotypic differentiation polymorphisms could then evolve into geneti- across unrelated taxa (convergence), (2) a test- cally differentiated populations if assortative able explanation of how the convergence con- mating occurs (Smith et al. 1997). Where upland fers a fi tness advantage, (3) a genetic basis for 132 STUDIES IN AVIAN BIOLOGY NO. 32 the phenotypic differences, and (4) a correlation georgiana nigrescens) bills in tidal marshes was between the magnitude of divergence in a char- signifi cantly greater than the bill volume of acter and the extent of time a particular taxa has the interior subspecies M. g. georgiana (Fig. 1). inhabited a particular ecosystem. They provided a short review of the literature for Seaside Sparrows, sharp-tailed sparrows CONVERGENCE IN BILL DIFFERENTIATION (Ammodramus caudacutus and A. nelsoni), Song IN TIDAL-MARSH PASSERINES Sparrows (Melospiza melodia), and Savannah Sparrows (Passerculus sandwichensis), point- Bill morphology is an evolutionarily labile fea- ing out that in each species the taxa found in ture in birds that is sensitive to selection due to tidal marshes have larger bills. Grenier and changes in foraging substrate or diet. Geographic Greenberg (2005) extended this line of study variation in bill size and shape can be an adaptive by measuring museum specimens from 10 spar- response to differences in food resources between row taxa endemic to tidal marshes, their closest habitats (Bardwell et al. 2001). Bill shape relates upland relatives, and 20 other taxa in the fam- to handling time and preferences for certain ily Emberizidae to determine the relationship foods (Hrabar et al. 2002). Bowman (1961) used between bill length, bill depth, and body mass functional analysis and correlations to show in these groups. Tidal-marsh birds tended to be that bill size and shape are intimately tied to the heavier and had signifi cantly longer and deeper proportion and size of seeds and invertebrates bills than their nearest kin outside of this habi- in the diet. Boag and Grant (1981) quantifi ed the tat. Even when differences in body size between selection intensity and corresponding change in the two groups were factored out, tidal-marsh bill depth when a drought caused a shift in the sparrows had longer bills (Fig. 2). Tidal-marsh size of seeds available to the Galápagos Medium sparrows had relatively longer bills with respect Ground-Finch (Geospiza fortis). While many of to bill depth as well. The authors also compared these studies focused on adaptations in bill depth tarsus length between tidal-marsh birds and sis- for seed-eating, bill length has been related to ter taxa, but found no signifi cant differences. speed of closure and, hence, the mobility of ani- These studies provide support for a new mal prey handled (Beecher 1962, Ashmole 1968, biogeographic rule (albeit one of limited Greenberg 1981). Bill size and shape are also taxonomic scope)—songbirds resident in tidal associated with the structures from which prey marshes have longer, narrower bills than inte- is captured (Bowman 1961). Thus, bill morphol- rior relatives. The basis of this rule is a trophic ogy is a likely trait to undergo adaptation to the adaptation, which stands in contrast to other trophic environment in tidal-marsh sparrows. established biogeographic rules (e.g., Allen’s Natural selection may also act upon leg and foot and Bergman’s) with physiological premises. proportions, perhaps to improve foraging effi - ciency (Schluter and Smith 1986). HYPOTHESIZED FUNCTION OF Murray (1969) found convergence in bill DIFFERENTIATED BILLS length of tidal-marsh Ammodramus taxa, and Greenberg and Droege (1990) showed that Based on our understanding of tidal-marsh the pattern of longer and overall larger bills food resources and the functional morphology in tidal marshes compared to non-tidal-marsh of passerine bills, we hypothesize that the dif- relatives extends to other sparrow genera. The ferentiation in bill size and shape is an adap- latter authors found that the overall volume tation for increased consumption of animal of Coastal Plain Swamp Sparrow (Melospiza foods, particularly marine invertebrates, and

FIGURE 1. From Greenberg and Droege (1990). Line drawings of typical adult male Melospiza georgiana geor- giana (a) and M. g. nigrescens (b). Note the longer bill and darker crown plumage of nigrescens. TROPHIC ADAPTATIONS—Grenier and Greenberg 133

FIGURE 2. From Grenier and Greenberg (2005). Relationship between culmen length and body mass for 36 taxa in Emberizidae. Tidal-marsh birds have longer bills relative to body mass, and bill length increases more quickly with body mass in tidal-marsh taxa. a concomitant decrease in eating seeds. Short, sparrows consume a broader diversity of prey deep bills are used for cracking large, hard than their upland kin by eating marine inver- seeds, while bird species with purely animal tebrates, possibly by the same mechanism of diets have long, thin bills (Beecher 1951). being able to extract them from crevices. These bills designed for carnivory are often As well as being useful for probing, long, used as forceps to probe for and capture inver- thin bills may be an adaptation to handle more tebrates in crevices under bark (Bowman 1961). mobile prey. Functional mechanics analysis Various researchers have proposed that tidal- indicates that the tips of longer bills can be marsh sparrows use their long bills to probe moved more quickly (Beecher 1962), and ecolo- for invertebrates in the sediment (Post and gists have surmised, therefore, that longer bills Greenlaw 1994, Allison 1995). In marshes fring- may close more rapidly on prey (Ashmole 1968), ing northern San Francisco Bay, amphipods making them more effi cient for capturing active (Traskorchestia traskiana) likely form a large prey (Greenberg 1981). Invertebrates are more part of the diet for the San Pablo Song Sparrow active than seeds, so the modifi ed bills of tidal- (Melospiza melodia samuelis; Grenier 2004). S. marsh sparrows may be adapted for effi ciently Obrebski and G. H. Irwin (unpubl. data) found capturing animal prey throughout the year. that these amphipods burrow into the substrate among the roots of the pickleweed (Salicornia TROPHIC OPPORTUNITIES AND virginica) or in cracks in the substrate during CHALLENGES IN TIDAL MARSHES neap-tide periods, probably to avoid desicca- tion. Long bills may be valuable for extracting Relatively few species of terrestrial verte- invertebrates such as amphipods from cracks brates reside in tidal marshes, despite the rich that form when the high marsh has not been food resources they offer (Chabreck 1988), sug- inundated for some time. A study of forest gesting that adaptation is required before tidal passerines (Brandl et al. 1994), concluded that marshes can be exploited successfully. The great- species with longer, less-deep bills consumed est challenge for terrestrial vertebrates invading a broader phylogenetic spectrum of prey taxa, tidal marshes is probably the high salt content of because they were able to extract new prey the food and water in these areas (Sabat 2000). types from under bark. Similarly, tidal-marsh Inability to adapt to hyper-saline conditions may 134 STUDIES IN AVIAN BIOLOGY NO. 32 exclude most songbird families from tidal-marsh coastal marshes (19%, N = 7). Nelson’s Sharp- residence. Salt tolerance, which mainly relates tailed Sparrow takes a wide variety of insects, to adaptations for processing the food after it is suggesting little specialization on particular eaten, is well documented for certain saltmarsh prey. The winter diet is not known. Contents sparrows and the salt marsh harvest mouse of Saltmarsh Sharp-tailed Sparrow stomachs (Goldstein, this volume; Fisler 1965). indicated a different trend in seasonal diet. Tidal marshes support an abundant inver- Although insects were important, the propor- tebrate community that includes marine taxa, tion was lower in the breeding season (44%, such as crustaceans, polychaetes, and mollusks, N = 20) and stayed about the same in the fall as well as terrestrial arthropods, mainly spiders (36%, N =12). However, plant matter, which and insects (Daiber 1982). In a study of the rela- was absent from the breeding diet, made up tionship between invertebrate abundance and only 30% of fall foods. A major addition to the avian foraging, Clarke et al. (1984) excluded diet (amphipods, 24% in both seasons) replaced birds from pools and the area around them in a summer insects and fall seeds for these tidal- Massachusetts saltmarshes in July and August, marsh sparrows (Greenlaw and Rising 1994). with little effect on the abundance of inverte- The Seaside Sparrow, an obligate tidal- brates in the exclosures. These data suggest that marsh species, consumes a diet similar to that invertebrate resources are extremely abundant of its close relative, the Saltmarsh Sharp-tailed at certain times of year relative to the needs Sparrow (Post and Greenlaw 1982). Also a gen- of avian predators, implying bottom-up rather eralist, the Seaside Sparrow eats insects, spiders, than top-down control of food resources. amphipods, mollusks, crabs, and marine worms The low plant-species diversity and the high during the breeding season and adds seeds as a degree to which perennial plants rely upon veg- major food source during winter (Martin et al. etative propagation results in a limited diver- 1961). Martin et al. (1961) took a small sample sity and abundance of seeds (Leck 1989) and no (N = 6) of stomachs from New Jersey late in the animal-dispersed fruits (Mitsch and Gosselink breeding season and found a heavy reliance on 2000) in tidal marshes. Based on studies on both marine invertebrates—36% crab and 24% snails North American coasts, Leck (1989) reported by volume. that few species were present in saltmarsh-soil Fewer data on Swamp Sparrow diet have seed banks (13–17 species) and seed abun- been published than for the other tidal-marsh dance was low (700–900 seeds/m2) compared songbirds. Like the upland Sharp-tailed to freshwater marshes and grasslands (30–40 Sparrows, inland Swamp Sparrows (Melospiza species, 1,000–3,000 seeds/m2). Furthermore, georgiana georgiana and M. g. ericrypta) consume regular tidal scouring of the substrate limits mainly insects during breeding and seeds dur- seed accumulation (Adam 1990). However, salt- ing fall and winter (Mowbray 1997). However, marsh plants are highly productive (Mitsch and the proportion of animal matter in the inland Gosselink 2000), so food resources are abundant Swamp Sparrow diet is relatively higher year- for herbivorous animals. round (Mowbray 1997). The diet of the tidal- marsh subspecies has not been studied, but PATTERNS IN THE DIET OF TIDAL-MARSH Greenberg and Droege (1990) suggest that these SPARROWS populations may consume marine invertebrates as a major food source. A comparison of diet by Greenlaw and The detailed summary of Savannah Sparrow Rising (1994) between the closely related diets by Wheelwright and Rising (1993) shows Nelson’s Sharp-tailed Sparrow (Ammodramus that this species follows the same pattern. The nelsoni), which breeds in the interior of the subspecies outside of tidal marshes consume continent as well as in tidal marshes, and insects, spiders, mollusks, seeds, and fruit, the Saltmarsh Sharp-tailed Sparrow, which with insects predominating during breeding breeds exclusively in tidal marshes, exempli- and seeds and fruit more important during fi es how the feeding niche differs in the tidal the off-season. A survey of 1,098 stomachs of marsh habitat. Stomach contents from Nelson’s breeding Savannah Sparrows from 31 localities Sharp-tailed Sparrows breeding in wet areas of across North America showed that crustaceans, New Brunswick and North Dakota, and migrat- which were present in 2% of the stomachs from ing along the East Coast of the US showed that upland locales, were found in 30% of the tidal these birds eat mainly insects (78% of relative marsh stomachs (predominantly fi ddler crabs total volume, N = 15) and spiders (14%) from [Uca]). Mollusks were also more frequent in May–August, with seeds becoming very impor- the stomachs of saltmarsh birds, and insects tant post-breeding (73%, N = 11), and some were less common than in the upland samples mollusks consumed during fall migration in (Wheelwright and Rising 1993). TROPHIC ADAPTATIONS—Grenier and Greenberg 135

The breeding season diet of non-tidal-marsh that in freshwater marshes, birds consumed Song Sparrows is dominated by a wide vari- large quantities of seeds, whereas birds in salt- ety of insects with the addition of a few other marshes fed almost entirely on invertebrates invertebrates and seeds, and seeds become the (Webster 1964). Similarly, the stomach contents main food source in fall and winter (Arcese of diamondback terrapins (Malaclemys terrapin), et al. 2002). Aldrich (1984) found that tidal- the only turtle specialized on saltmarshes, marsh Song Sparrows eat more animal mat- consist almost exclusively of marine mollusks ter than upland conspecifi cs, and this result (Ernst and Barbour 1989). was confi rmed by a stable-isotope study that Given that tidal marshes show strong simi- showed that San Pablo Song Sparrows from larity in vegetation to inland marshes and other a tidal marsh in northern San Francisco Bay habitats, we would expect species that are assimilated little, if any, plant matter during restricted to the vegetation layer to show less the breeding season (Grenier 2004). Behavioral pronounced diet shifts than those that use the data from the same study indicated that San marine substrate. Few data are available to test Pablo Song Sparrows fed heavily in areas where this prediction, but a small amount of informa- the abundant invertebrate biomass was marine tion seems to support the idea. Marsh Wrens snails and amphipods, and sparrows frequently (Cistothorus palustris) provide a good example carried amphipods to nestlings. Comparing the of a species that forages almost entirely from stomach contents of 233 Song Sparrows from a reed, grass, and shrub layers of the tidal marsh. variety of habitats around San Francisco Bay, The detailed study of diet by Kale (1965) for Marshall (1948a) found that the fall diet of the subspecies in Spartina marshes in Georgia saltmarsh birds continued to be mainly animals shows that Marsh Wrens consume primar- with the addition of some Grindelia seeds and ily insects and spiders, but a small portion of Spartina fl owers, while brackish marsh and stomach samples contained invertebrates, such terrestrial populations consume mainly seeds as crabs and amphipods, as well as snails asso- supplemented by insects. ciated with the marine substrate. A comparison In summary, tidal-marsh sparrows and their with studies of interior populations (Beal 1907, close relatives are generalists that consume both Welter 1935) in New York state and California animal matter and seeds. However, tidal-marsh suggest interesting differences between tidal- birds tend to eat a greater proportion of inverte- and freshwater -marsh populations that should brates and a correspondingly lesser proportion be explored. Kale (1965) found that ants and of seeds than their inland relatives. This differ- spiders were larger components of the breed- ence may be most pronounced in autumn and ing season diet of the Marsh Wrens in salt- winter. Tidal-marsh sparrows also consume marshes than freshwater marshes, where the more marine invertebrates and fewer insects diet was dominated by Orthoptera, Odonata, and spiders than upland sparrows. and Lepidoptera. Specialized forms of tidal-marsh mammals TROPHIC PATTERNS IN OTHER TIDAL- are restricted to a few rodents. Rodent grani- MARSH VERTEBRATES vores give way to herbivores in tidal marshes. Common tidal-marsh rodents include muskrats Beyond sparrows, few studies have focused (Ondatra zibethicus), California voles (Microtus on trophic specialization in tidal-marsh ver- californicus), and meadow voles (M. pennsylva- tebrates. As discussed in detail for sparrows, nicus) which are predominantly herbivorous the available data suggest that other birds in (Thaeler 1961, Willner et al. 1980, Batzli 1986). tidal marshes reduce consumption of seeds in Consistent with the dominance of herbivory favor of increased use of invertebrates, includ- in saltmarsh mammals, the salt marsh harvest ing intertidal taxa. Clapper Rails, which dwell mouse, which is endemic to tidal marshes, con- in saltmarshes, and King Rails (Rallus elegans), sumes considerably more plant material than which prefer brackish to freshwater marshes, does its closest relative, the western harvest both feed predominantly on animal matter, mouse (Reithrodontomys megalotis) in uplands particularly crustaceans. However, King Rails (Fisler 1965). Fisler (1965) demonstrated that (as well as freshwater populations of the Yuma the salt marsh harvest mouse has a substan- Clapper Rail [R. l. yumanensis]) eat much larger tially longer digestive tract than the upland quantities of insects and seeds than do Clapper species, which is likely an adaptation for Rails, particularly in the autumn and winter digesting a greater proportion of plant material (Meanley 1992). Meanwhile, saltmarsh Clapper in the diet. Absent among rodents commonly Rails eat primarily crabs and snails (Eddleman found in tidal marshes are granivorous and fru- and Conway 1998). A study of the fall diet of givorous species (Greenberg and Maldonado, Soras (Porzana carolina) in Connecticut showed this volume). 136 STUDIES IN AVIAN BIOLOGY NO. 32

Carnivory is also prevalent in small mammals Seaside Sparrow (Ammodramus maritimus in tidal marshes. Shrews, a common component nigrescens) exhibited distinctly melanistic plum- of tidal-marsh faunas, are specialists on inver- age. Saltmarsh Sharp-tailed Sparrows are more tebrates, and indirect evidence suggests that at heavily streaked with fewer white markings least one specialized tidal-marsh subspecies of dorsally than Nelson’s Sharp-tailed Sparrows, the ornate shrew (Sorex ornatus sinuosus; Hays and Ammodramus nelsoni subvirgatus in tidal and Lidicker 2000) feeds on amphipods. The marshes of the Canadian maritime provinces restriction in diet guilds to herbivores and car- are grayer than conspecifi cs from interior prai- nivores may result from fi ltering of colonizing ries (Ridgway and Friedmann 1901, Greenlaw species (e.g., shrews are more likely to colonize and Rising 1994). The streaking of Belding’s marshes because they are carnivores), or it Savannah Sparrow is heavier and darker than may result from niche shifts. Marsh rice rats typical Savannah Sparrows, but the large-billed (Oryzomys palustris), common in tidal marshes subspecies are distinctly pale, although gray- of the southeastern US (Daiber 1982, Wolf 1982) ish in tone (Ridgway and Friedmann 1901, are known to depend heavily on invertebrates, Wheelwright and Rising 1993). A quantitative particularly from the benthic substrate (Sharp study of variation in Song Sparrow dorsal 1967). Comparison of stomach contents between plumage (Marshall 1948b), found upland rats in tidal marsh and the immediately adjacent Melospiza melodia gouldii to be reddish-brown, uplands (Kruchek 2004) showed that tidal-marsh while tidal-marsh subspecies maxillaris, samuelis rice rats consume far more invertebrates and and pusillula were blackish-brown, blackish- less plant material than those in the adjacent old olive, and yellowish-gray, respectively. Swamp fi elds. Even in the grass-specialized herbivore, Sparrows in tidal marshes also lose their color- the California vole, stable-isotope analysis of ful rusty tones dorsally, and rusty crown and the spring pelage of an individual captured in nape plumage is replaced with black feathers saltmarsh revealed a diet based completely on (Greenberg and Droege 1990). animal foods (Grenier 2004). Saltmarsh melanism, or the tendency to be grayer or blacker, has been reported for sev- DORSAL COLOR SPECIALIZATION FOR eral other birds as well (Table 1). The weaker FORAGING IN TIDAL MARSHES plumage differentiation in Marsh Wrens is not surprising given that foraging in this species Another less apparent feeding-related adap- is more associated with water edge and veg- tation to a new habitat is cryptic coloration to etation rather than open sediment (Kroodsma reduce predation risk while foraging. Tidal- and Verner 1997). In addition to these avian marsh sparrows and their close relatives in the examples, saltmarsh melanism has been upland forage mainly along the sediment and observed in various small mammals, namely in low foliage, obtaining food from near to or cinereus shrew (Sorex cinereus), ornate shrew (S. on the ground (Wheelwright and Rising 1993, ornatus), vagrant shrew (S. vagrans), California Greenlaw and Rising 1994, Post and Greenlaw vole, meadow vole, and western harvest mouse 1994, Mowbray 1997, Arcese et al. 2002). Often (Grinnell 1913, Jackson 1928, Green 1932, Von they are observed foraging on the exposed sur- Bloeker 1932, Rudd 1955, Hall and Kelson 1959, face of tidal channels and sloughs. Thus, dorsal Thaeler 1961, Fisler 1965, Woods et al. 1982), coloration that matches the background color of and in one tidal-marsh snake (Nerodia sipedon the sediment may be important for reducing the williamengelsi; Conant et al. 1998) risk of predation. For tidal-marsh sparrows, the It was long ago hypothesized (Grinnell 1913, periodic exposure by the tide of unvegetated Von Bloeker 1932) that the blackest forms of sediment provides both a novel foraging sub- tidal-marsh species were found in brackish strate and a new predation risk, so selection for upper estuaries (such as Suisun Bay in the San cryptic dorsal plumage is plausible. Francisco estuary). This hypothesis is borne out Grinnell (1913) noted that tidal-marsh ver- by the following melanistic vertebrate taxa: tebrates tend to be darker than their upland Coastal Plain Swamp Sparrow, Suisun Song relatives, and Greenberg and Droege (1990) Sparrow (Melospiza melodia maxillaris), Dusky reviewed this phenomenon, noting that the Seaside Sparrow, Suisun shrew (Sorex ornatus trend is sometimes more toward grayer hues sinuosis), and tidal-marsh populations of the rather than darker coloration. Saltmarsh California vole. melanism is clearly expressed within the tidal- The blacker and grayer dorsal coloration of marsh sparrows. Seaside Sparrows can be dis- tidal-marsh vertebrates may be an adaptation tinguished from other sparrow species in the for blending in against the sediment background fi eld by their dark olive-gray dorsal coloration to reduce the risk of predation while foraging (Sibley 2000), and the recently extirpated Dusky in the open. Relative to reddish sediment in TROPHIC ADAPTATIONS—Grenier and Greenberg 137

TABLE 1. COMPARISON OF PLUMAGE COLORATION OF TIDAL-MARSH-BIRD TAXA WITH THEIR CLOSEST NON-TIDAL-MARSH RELATIVES.

Tidal-marsh taxon Taxon for comparison Coloration in tidal marsh Clapper Rail (East Coast; Rallus longirostris King Rail (Rallus elegans) Grayer. crepitans group) Clapper Rail (West Coast; R. l. obsoletus group) King Rail Somewhat grayer. Marsh Wren (Cistothorus palustris griseus) Marsh Wren, non-tidal marsh Only griseus (southern and other tidal-marsh populations populations Atlantic coast) is distinctly grayer. Suisun Song Sparrow (Melospiza melodia Modesto Song Sparrow Grayer with blacker maxillaries) (M. m. mailliardi) markings. Alameda Song Sparrow (M. m. pusillula) Heermann’s Song Sparrow Grayer. (M. m. heermanni) San Pablo Song Sparrow (M. m. samuelis) Marin Song Sparrow (M. m gouldii) Grayer. Coastal Plain Swamp Sparrow (M. georgiana Southern Swamp Sparrow Grayer with blacker nigrescens) (M. g. georgiana) markings. Belding’s Savannah Sparrow (Passerculus Savannah Sparrow (P. sandwichensis): Grayer with blacker sandwichensis beldingi group) interior subspecies markings. Large-billed Savannah Sparrow (P. s. Savannah Sparrow (P. sandwichensis): Grayer. rostratus group) interior subspecies Saltmarsh Sharp-tailed Sparrow (Ammodramus Nelson’s Sharp-tailed Sparrow Grayer. caudacutus) (A. nelsoni) Acadian and James Bay Sharp-tailed sparrows Nelson’s Sharp-tailed Sparrow Grayer wings, less (A. n. subvirgatus and A. n. alterus) (A. n. nelsoni) contrasting back.

terrestrial habitats, tidal marsh mud is grayer. infl uence on bill shape in Red-winged Blackbirds This phenomenon occurs because sea water is (Agelaius phoeniceus) by cross fostering nestlings rich in sulfates, and, in the anoxic conditions between geographic areas with morphologi- of tidal sediment, iron is reduced anaerobically cally distinct populations. Other studies show to grayish iron sulfi des rather than to the red- that bill size and shape are largely heritable dish iron oxides of aerobic soils (Mitsch and (Boag and Grant 1981, Forstmeier et al. 2001). Gosselink 2000). The blacker coloration of birds Given that Smith and Zach (1979) found Song and mammals in brackish marshes may be a Sparrow bill traits to be signifi cantly heritable, result of background matching to blacker sedi- we proceed with the assumption that the bill ments. Upper estuary mud may have a greater morphology of tidal-marsh sparrows is deter- quantity of dark organic materials relative to mined mainly by genetics. While heritability of saltmarsh sediments, due to the closer proxim- bill morphology would make this trait poten- ity of riverine inputs (Odum 1988). tially sensitive to selection, low heritability does The Alameda Song Sparrow (Melospiza not rule out the possibility that differentiation melodia pusillula) and the large-billed Savannah at the subspecies and species levels is geneti- Sparrow group (Passerculus sandwichensis cally based (Merilä and Sheldon 2001). rostratus and related subspecies) are partial The heritability of plumage coloration is not a exceptions to the general trend of tidal-marsh simple question, because different feather colors melanism. Although both are relatively pale, are controlled by different mechanisms. A gene they have grayish dorsal coloration, which is was recently identifi ed that likely controls mel- consistent with other tidal-marsh forms. Both anin deposition in Bananaquits (Coereba fl ava; sparrows inhabit the most saline and arid Theron et al. 2001), and this gene or a number of marshes of their respective regions. This corre- other loci identifi ed in poultry may contribute lation suggests background matching to a paler to increased melanin expression in tidal-marsh color for camoufl age in drier, saltier marshes. songbirds. Greenberg and Droege (1990) raised 11 Coastal Plain Swamp Sparrow nestlings ENVIRONMENTAL AND GENETIC taken from the wild at 4–6 d old in the lab under CONTRIBUTIONS TO TIDAL-MARSH standardized conditions. When measured after ADAPTATIONS the postjuvenal molt, these birds were similar in both dorsal color and bill size to adult Coastal Both environment and genes likely play a Plain Swamp Sparrows and distinct from inland role in determining bill morphology. James Swamp Sparrows. Although more experiments (1983) found a surprisingly large environmental are required, this result suggests that bill 138 STUDIES IN AVIAN BIOLOGY NO. 32

morphology and plumage color have large heri- table components in tidal-marsh sparrows.

EVIDENCE FOR A TAXON CYCLE IN TIDAL- MARSH SPARROWS

Generally only one or two sparrow species can be found breeding in the same tidal marsh. The exception occurs along the mid-Atlantic seaboard, primarily Chesapeake and Delaware bays. In these estuaries, three species cohabit tidal marshes—two saltmarsh specialists, Seaside Sparrow and Saltmarsh Sharp-tailed Sparrow, joined by the Coastal Plain Swamp Sparrow. Genetic data suggest a very recent colo- nization of the brackish upper estuary by Swamp Sparrows (Greenberg et al. 1998) in contrast to FIGURE 3. From Grenier and Greenberg (2005). a much longer association with tidal marshes in Relationship between the difference in culmen length the other species indicated by a deep divergence and the difference in body mass between sister taxa in from upland relatives (Zink and Avise 1990). We different habitats. Differences are the mean for tidal- suggest that coastal marshes existed along the marsh birds minus the mean for the upland relative. gently sloping continental shelf of the eastern Divergence is classified as either recent (<10,000 ybp) seaboard throughout the Pleistocene, allowing or ancient (>200,000 ybp). the more specialized Ammodramus sparrows to persist in saltmarshes (Malamud-Roam et al., this few thousand years old (Suisun Song Sparrow; volume). The more recent development of estua- Atwater et al. 1979). rine marshes (Malamud-Roam et al., this volume) may have allowed Swamp Sparrows from small FUTURE RESEARCH inland populations, which were expanding as the most recent continental glaciers receded Although the patterns that we have dis- (Greenberg et al. 1998), to colonize these brack- cussed are compelling, rigorous fi eld stud- ish areas that were less suited to the adaptations ies are required to empirically test if they of Seaside and sharp-tailed sparrows. refl ect adaptation to tidal marshes. In variable Support for this idea that adaptive special- environments like tidal marshes, natural selec- ization for the tidal-marsh environment accrues tion acts in concentrated bursts to carve the over evolutionary time is provided by the cor- evolutionary paths of populations (Benkman relation between morphological divergence 1993), and for trophic adaptations the epi- and genetic divergence in tidal-marsh sparrows sodes of selective change are probably related (Fig 3; Grenier and Greenberg 2005). The four to resource scarcity (Boag and Grant 1981, tidal-marsh sparrows with ancient divergence Schluter and Smith 1986). Therefore, studies times from their upland counterparts (>200,000 are needed that track the distribution of feed- yr BP) exhibited signifi cantly more extreme ing-related traits in a tidal-marsh population bill elongation than recently diverged groups concurrent with the survival and reproductive (<10,000 yr BP). We suspect that divergence success of individuals and the abundance of will increase in the younger taxa as enough resources. Tidal-marsh passerines may be trac- time passes for benefi cial mutations to accu- table systems for attempting this type of real- mulate and be selected. The type of tidal-marsh time measurement of natural selection, because habitat each taxon inhabits is not a confound- populations are often dense enough to provide ing factor in this analysis; saltmarsh specialists large sample sizes. More knowledge of the tro- are found in both the ancient (Seaside Sparrow, phic ecology of tidal-marsh songbirds, particu- Savannah Sparrow, Saltmarsh Sharp-tailed larly when and how they experience resource Sparrow) and recent (San Pablo Song Sparrow scarcity, would be a fi rst step. Also, a better and Alameda Song Sparrow [Melospiza melodia understanding of saltmarsh food resources, par- pusillula]) divergence groups. Brackish-marsh ticularly invertebrate and seed distribution and specialists are found only in the recent diver- abundance, is needed. Finally, cross-fostering gence group, either in sympatry with other experiments between upland and tidal-marsh tidal-marsh sparrows (Coastal Plain Swamp subspecies would shed light on the importance Sparrow), which fi ts with the proposed taxon of environment in creating the patterns we have cycle, or in relatively young marshes only a reviewed. TROPHIC ADAPTATIONS—Grenier and Greenberg 139

ACKNOWLEDGMENTS work on tidal-marsh birds and for manuscript preparation was provided by the Abbott Fund Thanks to S. R. Beissinger, E. Lacey, C. of the Smithsonian Institution, the Delaware Benkman, and B. Eddleman for constructive Ornithological Society, the San Francisco Bay reviews of earlier drafts of the chapter and Fund, the Budweiser Conservation Scholarship, to the American Museum of Natural History the P.E.O. Scholar Award, the Garden Club of and the Museum of Vertebrate Zoology, America Award in Coastal Wetlands Studies, University of California, Berkeley, for access the Phi Beta Kappa Fellowship, and the Joseph to specimens. Financial support for fi eld Mailliard Fellowship in Ornithology. REGIONAL STUDIES

Clapper Rail (Rallus longirostris) with fi ddler crab (Uca pugnax) Drawing by Julie Zickefoose