Indirect Effects of Feral Horses on Estuarine Communities

PHILLIP S. LEVIN,*‡ JULIE ELLIS,* RACHEL PETRIK,* AND MARK E. HAY† *Institute of Marine Science, University of California, Santa Cruz, Santa Cruz, CA 95064, U.S.A. †Institute of Marine Sciences, University of North Carolina, Morehead City, NC 28857, U.S.A.

Abstract: Livestock have grazed on salt marshes for centuries and have dramatic effects on marsh vegeta- tion. Most studies examining the effects of livestock on salt marshes have focused on the effects on plants rather than on salt marsh fauna or ecological processes. However, grazers such as feral horses may have strong indirect effects on communities by altering the habitat, making it more or less suitable for species that potentially occur there. We evaluated the indirect effects of grazing by feral horses on estuarine animals that use salt marshes and adjacent subtidal communities. Surveys revealed that horse-grazed marshes had less vegetation, a higher diversity of foraging birds, higher densities of crabs, and a lower density and species rich- ness of fishes than marshes not grazed by horses. In addition, fish density was reduced in subtidal habitats adjacent to grazed marshes. Experiments manipulating marsh vegetation indicated that the potential for pre- dation on fishes in ungrazed marshes was higher than in grazed marshes. Results of additional experiments in which fishes were enclosed with or without artificial Spartina suggested that the removal of shelter pro- vided by marsh vegetation results in behavioral shifts by fishes that make them more susceptible to preda- tion. Although large herbivores are naturally absent from extant salt marsh ecosystems, such large herbivores were common members of Pleistocene communities. Using modern horses as surrogates for extinct ungu- lates, we hypothesize that large herbivores could have had strong indirect effects on Pleistocene estuarine habitats. We argue that both the modern introduction of ungulates to salt marshes and the prehistoric elimi- nation of large herbivores affected estuarine biodiversity.

Efectos Indirectos de Caballos Silvestres en Comunidades de Estuario Resumen: El ganado ha pastado en las marismas por siglos y tiene efectos dramáticos en la vegetación. La mayoría de los estudios que examinan los efectos del ganado en las marismas se han centrado más en los efectos sobre las plantas que sobre la fauna de la marisma o los procesos ecológicos. Sin embargo, los her- bívoros como caballos silvestres, pueden tener fuertes efectos indirectos en comunidades alterando el hábitat haciéndolo más o menos adecuado para las especies que potencialmente ocurren ahí. Evaluamos los efectos indirectos del pastoreo por caballos silvestres en los animales estuarinos que utilizan marismas y las comu- nidades inframareales adyacentes. Los muestreos revelaron que las marismas pastoreadas por caballos tenían menos vegetación, una mayor diversidad de aves forrajeras, mayor densidad de cangrejos, y menor densidad y riqueza de especies de peces que las marismas no pastoreadas por caballos. Además, la densidad de peces fue reducida en los hábitats inframareales adyacentes a las marismas pastoreadas. Experimentos de manipulación de la vegetación de marisma indicaron que el potencial de depredación de peces en marismas no pastoreadas fue mayor que en las marismas pastoreadas. Los resultados de experimentos adicionales en los que peces fueron encerrados con o sin Spartina artificial sugirieron que el retiro del abrigo proporcionado por la vegetación del marisma da lugar a cambios de comportamiento de peces que los hacen más suscepti- bles a la depredación. Aunque los herbívoros mayores están naturalmente ausentes de los ecosistemas de ma- risma existentes, tales herbívoros eran miembros comunes de comunidades del Pleistoceno. Usando caballos

‡Current address: Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Boulevard E., Seattle, WA 98112, U.S.A., email [email protected] Paper submitted April 6, 2001; revised manuscript accepted September 26, 2001. 1364

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Levin et al. Effects of Feral Horses on Estuarine Habitat 1365 modernos como sustitutos de los ungulados extintos, presumimos que los herbívoros grandes habrían podido tener fuertes efectos indirectos en hábitats estuarinos del Pleistoceno. Proponemos que tanto la introducción moderna de ungulados a las marismas y la eliminación prehistórica de herbívoros mayores afectaron a la biodiversidad de los estuarios.

Introduction moved from the island by the U.S. National Park Service, leaving horses as the only feral ungulates on Shackleford In temperate coastal zones throughout the world, salt Banks (Wood et al. 1987). Horse numbers peaked in marshes fuel a tremendous engine of biological produc- 1994 at 225 and, after being culled by the National Park tivity. The grasses and rushes of the salt marsh sprawl Service, dropped to 108 in 1997. Spartina alterniflora, across expanses of intertidal mud and sand, producing the dominant low marsh plant, comprises 50% of the nearly as much carbon per unit area as tropical rain for- diet of feral horses on Shackleford Banks and is their ests (Whittaker 1975). This productivity is typically ex- most important food item (Wood et al. 1987). Horse ported to adjacent estuarine and nearshore waters, sus- grazing causes large decreases in standing biomass, per- taining dense populations of fishes and invertebrates cent cover, blade height, culm density, seed production, (Adam 1990). The lush vegetation of marshes also cre- and belowground biomass of Spartina (Turner 1987; ates a biogenic refuge from predation, allowing many ju- Wood et al. 1987; Furbish & Albano 1994). Because venile fishes and invertebrates to thrive on the marsh Spartina forms a near monoculture in the low marsh, surface at high tide (Minello 1999). salt marshes that are grazed by horses have vastly differ- Although many ungulates (Camelidae, Bovidae, Equidae) ent plant assemblages than marshes that are inaccessible and Proboscids (Mammuthus columbi) grazed Pleistocene to horses (Hay & Wells 1991; Furbish & Albano 1994). marshes (Koch et al. 1998), extant salt marshes differ Most studies examining the effects of ungulate grazers from most ecosystems in that herbivores play only a mi- on salt marshes have focused on the direct effects on nor role in structuring the community (Adam 1990). In plants rather than on the indirect effects of grazing on salt most cases, the dominant herbivores in marshes are in- marsh fauna, faunas of associated communities, or eco- sects, although seasonal aggregations of geese can impose logical processes. Grazers such as the feral horses of locally intense grazing pressure (Smith & Odum 1981; Shackleford Banks may have strong indirect effects on Adam 1990). Rates of plant consumption by insects are communities by altering the habitat, making it more or small relative to plant production, and only a fraction less suitable for species that potentially occur there. of salt marsh primary production is consumed directly Here, we evaluated the indirect effects of horse grazing (Adam 1990). Most production thus enters marsh and on the saltmarsh and adjacent subtidal community of adjacent subtidal food webs via detrital processes (Adam Shackleford Banks by comparing marsh islands that did 1990). or did not experience horse grazing. Because of their im- Although natural grazers are relatively unimportant in portance in salt marsh food webs (Adam 1990), we fo- structuring salt marshes, livestock have grazed on salt cused our efforts on birds, fishes, and crabs, and asked marshes for centuries (Nixon 1980). Livestock grazing how their abundance was affected by horse grazing. We can reduce net primary productivity, decrease above- then extended these measured effects of extant feral and belowground biomass, and decrease plant height horses to shed light on the effects that extinct megaher- (Petrides 1975; Dijkema 1990). Livestock grazing on salt bivores may have had on estuarine communities in the marshes also may alter energy flow by reducing the Pleistocene. build-up of detritus (Adam 1990) and by changing detri- tal dynamics in ways that alter net production available for transport to adjacent estuarine waters. Methods In colonial America, introduction of ungulates to bar- rier islands by European explorers and immigrants was a We selected as our study sites six marsh islands of about common practice (Petrides 1975). Europeans colonized 10 km2 each that were adjacent to Shackleford Banks. Shackleford Banks, a 923-ha barrier island near Beaufort, Three of these islands were accessible to horses because North Carolina, about 210 years ago, bringing horses, they were separated from the main island by shallow cattle, sheep, goats, and pigs with them (Lewis 1917). waters that did not prevent horses from wading to and When the settlers departed in the late 1800s, livestock grazing on them. Three islands were not visited by were left behind (Engels 1952). During the late 1980s, horses because of deeper water that deterred horses. Is- the remaining cattle, sheep, goats, and pigs were re- lands were separated from one another by 0.5–1.5 km.

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Previous descriptive and long-term experimental studies each experimental plot. The experiment was conducted in marshes show that horses significantly decrease Spar- at high tide, and water depth was about 50 cm. At 30- tina abundance at sites to which they have access minute intervals, we counted the number of fish remain- ( Wood et al. 1987; Hay & Wells 1991). ing until no fish remained in one of the treatments or un- To document bird usage and density on each island, til the experiment was terminated (after 180 minutes). we performed scan samples using binoculars from a sta- We stopped the experiment when the tide ebbed and tionary boat. Our methodology followed standard proce- fish normally would have moved off the marsh surface. dures as described by Altman (1974) and used with suc- F. heteroclitus is an extremely hardy fish, and tethering cess in previous studies of birds in marine intertidal of F. heteroclitus has been successfully employed in nu- habitats (e.g., Irons et al. 1986; Marsh 1986). During merous previous investigations to investigate habitat- each sample we noted the abundance of all birds by spe- specific rates of predation (e.g., Rozas & Odum 1987; cies. We also recorded numbers of birds foraging, flying McIvor & Odum 1988; Ruiz et al. 1993). But because above the island, standing still, and nesting at both tethering fish can affect habitat treatments such as ours, horse-grazed and ungrazed marshes. We sampled each caution is clearly warranted in the interpretation of such of the islands on four occasions during both high and studies (Peterson & Black 1994; Curran & Able 1998). low tides, and the order in which islands were visited Consequently, we performed a second experiment to was randomized. further examine the mechanisms underlying patterns of Using conical, galvanized-steel, wire-mesh minnow habitat use by F. heteroclitus. traps (42 cm long, 22.5 cm maximum diameter, 3.5 cm In our second experiment, we tested the effects of res- entrance diameter), we sampled fish at the marsh sur- ident crabs as predators on fish by constructing enclo- face. At 3-week intervals from June through August sures to hold transplanted fish and resident crabs but to 1997, 15 unbaited traps were placed at about 1.5-m in- exclude birds and other larger consumers. On a horse- tervals along the low tide line. Traps were retrieved after grazed marsh, we built 16 (2 2 1 m) enclosures of 10 hours during the following falling tide. All fishes were vexar screening (0.64-cm mesh) with the bottom edge released where they were captured. In preliminary sur- of the enclosures buried 15–20 cm in the sediment and veys, the rank order of pinfish (Lagodon rhomboides) with a fitted top (2.54-cm mesh) to exclude birds. In half among subtidal sites adjacent to our marsh sites was sim- of the enclosures (n 8) we added 300 bamboo poles ilar whether we sampled with minnow traps, throw per square meter to simulate the presence of Spartina. traps, or otter trawls (Petrik & Levin 2000). We chose to Bamboo poles were approximately evenly spaced use minnow traps because of their ease of use and our within enclosures. Controls (n 8) consisted of enclo- ability to sample all sites concurrently. To sample juve- sures without poles. To provide a low-tide refuge for nile fishes and xanthid crabs, we placed 10 pit traps at fish in our enclosures, we buried plastic containers each site (Kneib 1984). Pit traps were fashioned from within each enclosure such that the top of the container 1.5-L plastic containers custom fit into pits dug 50 cm was flush with the marsh surface. We constructed enclo- from the marsh edge. As the tide ebbed, resident salt- sures at low tide so that all transient predators were ex- marsh fishes retreated to the pools of water created by cluded from the experimental plots, and mud crabs the traps. Pit traps were sampled weekly from 15 June (Sesarma spp.) were the only potential fish predator to 31 August 1997. present (Kneib 1986). We then added three mummi- To test if horse removal of Spartina affects predation chogs (1 SD above the mean number of fish we sampled on marsh-associated fishes, we performed two experi- at these sites) to each enclosure 2 hours before a day- ments with a common marsh fish, the mummichog light high tide, and we counted the number of fish re- (Fundulus heteroclitus). We examined predation rates maining about 20 hours later at the next daylight low on tethered fish in plots where we simulated grazing tide. We repeated this experiment twice. (n 12) of Spartina and in control plots where Spar- tina was left intact (n 12). We simulated grazing in 16-m2 plots of ungrazed marsh by clipping aboveground Results biomass of Spartina with hedge clippers. We clipped as close to the substrate as possible, and our manipulated Eighty percent of the 663 birds observed in our sur- patches were close in appearance to areas recently veys used ungrazed marshes (Table 1; Fig. 1). In particu- grazed by horses. lar, Laughing Gulls (Larus atricilla) and Forster’s Terns Paired with these plots were controls in which Spar- (Sterna fosteri ) nested in great abundance in ungrazed tina was not manipulated. In each treatment and control marshes and dominated the avian assemblage there (96% plot, a single mummichog was attached to a 1-m-long of the total). However, Laughing Gulls were virtually tether. Tethers were looped loosely around bamboo absent and Forsters’ Terns significantly reduced in num- poles that had been forced into the substrate. This al- bers on marshes grazed by horses (Table 2; Fig. 1). Wil- lowed the fish to swim in a 3.14-m2 area in the center of lets (Catoptrophorus semipalmatus) and Least Sand-

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Table 1. The number, percent, and diet of birds observed in horse-grazed and ungrazed marshes.

No. of birds (%) No. of in birds (%) horse-grazed in ungrazed Species, scientific name marshes marshes Diet Willet, Catoptrophorus semipalmatus 38 (28.8) 2 (0.38) crabs (Uca and Sesarma spp.) (Tomkins 1965) Least Sandpiper, Calidris minutilla 21 (15.9) 0 benthic invertebrates (Cooper 1994) Forster’s Tern, Sterna fosteri 20 (15.1) 191 (36.0) mostly fish, some crustaceans in shallow, open water (Martin & Zwank 1987) Ruddy Turnstone, Arenaria interpres 9 (6.8) 0 benthic invertebrates (Michaud & Ferron 1990) White Ibis, Eudocimus albus 8 (6.1) 1 (0.2) crabs (Uca and Panopeus spp.) (Kushlan & Bildstein 1992) Short-billed Dowitcher, Limnodromus griseus 3 (2.3) 0 polychaetes (Weber & Haig 1997) Whimbrel, Numenius phaeopus 3 (2.3) 2 (0.38) crabs (Turpie & Hockey 1997) Marbled Godwit, Limosa fedoa 3 (2.3) 0 benthic invertebrates (Dodd & Colwell 1998) Laughing Gull, Larus atricilla 3 (2.3) 321 (60.5) inland generalist predator and opportunistic scavenger (Dosch 1997) Black-bellied Plover, Pluvialis squatarola 3 (2.3) 0 polychaetes and crustaceans (Michaud & Ferron 1990) Herring Gull, Larus argentatus 3 (2.3) 0 generalist predator and opportunistic scavenger (Pierotti & Good 1994) Red Knot, Calidris canutus 3 (2.3) 0 bivalves (Cummings et al. 1997) Snowy Egret, Egretta thula 3 (2.3) 0 fish and crustaceans (Willard 1977) Great Egret, Casmerodius albus 2 (1.5) 1 (0.2) fish (Willard 1977) Yellow-crowned Night-Heron, Nycticorax violaceus 2 (1.5) 0 crabs, mostly Uca (Watts 1988) Spotted Sandpiper, Actitis macularia 2 (1.5) 0 generalist predator on small animals (Oring et al. 1997) Black-Crowned Night-Heron, Nycticorax nycticorax 2 (1.5) 0 opportunistic predator (Davis 1993) Boat-tailed Grackle, Quiscalus major 2 (1.5) 10 (1.9) — Sanderling, Calidris alba 2 (1.5) 0 benthic invertebrates (Connors et al. 1981) Black Skimmer, Rynchops niger 0 2 (0.38) fish (Black & Harris 1983) Great Blue Heron, Ardea herodias 0 1 (0.2) fish (Willard 1977) Total 132 531

pipers (Calidris minutilla) were the most common bird 2), although juvenile mummichogs were captured only species we observed using grazed marshes, and both in ungrazed marshes (x 1.11 per pit trap; SE 0.56). species were nearly absent from ungrazed marshes ( Ta- Similarly, pinfish were completely absent from grazed ble 2; Fig. 1). Although the number of individual birds marshes (Fig. 2). Xanthid crab (Sesarma reticulatum) abun- we surveyed was significantly greater in ungrazed than dance averaged 5.56 (SE 1.33) per pit trap in grazed in grazed marshes (Table 2; Fig. 1), we observed twice marshes versus 2.14 (SE 0.37) in ungrazed marshes (t as many bird species in horse-grazed than in ungrazed 3.115; p 0.006). marshes (20 vs. 10 species, respectively) (Table 1; Fig. In our tethering experiment, more than 80% of fish 1). Of the 20 species we observed in horse-grazed were eaten in plots in which grazing was simulated, marshes, 17 (85%) were species that typically forage on whereas 20% were consumed in control plots (Z benthic invertebrates in unvegetated or sparsely vege- 2.84, p 0.001; Fig. 3). In all cases where fish were con- tated estuarine habitats (Table 1). During our scan sam- sumed, we observed fish seeking shelter in holes in the ples in horse-grazed marshes, an average of 31% (SE marsh surface occupied by xanthid crabs, making the 0.11) of birds were actively foraging per scan, whereas fish easy prey for the crabs. Fish did not seek shelter we saw no birds foraging in ungrazed marshes. in crab holes when Spartina was available. Similarly, in Fish abundance and species richness were signifi- plots in which we added poles to simulate the presence cantly higher in ungrazed marshes than in grazed of Spartina, 85% of the fish survived, whereas only 28% marshes (Fig. 2). Two fish species, mummichogs and of the fish survived in control plots (t 3.79, p 0.001; pinfish, dominated our samples (18% and 76%, respec- Fig. 3). Because birds were excluded from our enclo- tively). Adult mummichog abundance averaged 14 times sures and the enclosures were erected at low tide, the higher in ungrazed than in horse-grazed marshes (Fig. only predators with access to enclosed fish were those

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Table 2. Analysis of variance on the effects of tidal state (tide, T), the presence or absence of feral horses (horse, H), and their interaction (T*H) on the dominant species of birds, total number of birds, and bird-species richness.

Sum of Degrees of Mean Source squares freedom square F ratio p Laughing Gull tide 1.29 1 1.29 0.84 0.37 horse 10.53 1 10.53 6.83 0.01 T*H 1.03 1 1.03 0.67 0.42 error 58.52 38 1.54 Forsters’ Tern tide 2.54 1 2.54 1.99 0.17 horse 8.76 1 8.76 6.86 0.01 T*H 0.16 1 0.16 0.12 0.73 error 48.51 38 1.54 Willet tide 0.15 1 0.15 0.41 0.53 horse 2.88 1 2.88 7.74 0.009 T*H 0.33 1 0.33 0.89 0.35 error 13.78 38 0.37 Sandpiper tide 0.98 1 0.98 4.96 0.03 horse 2.74 1 2.74 13.86 0.006 T*H 0.98 1 0.98 4.97 0.03 error 7.51 38 0.20 All bird species tide 1.91 1 1.91 2.37 0.13 horse 4.82 1 4.82 5.97 0.02 T*H 5.83 1 5.83 7.23 0.01 error 30.68 38 0.81 Species richness tide 0.11 1 0.11 0.99 0.33 horse 2.34 1 2.34 21.40 0.001 T*H 1.28 1 1.28 11.70 0.002 error 4.16 38 0.11

to a species-rich assemblage of foraging shore birds. At Figure 1. Mean number of birds in scan samples con- our study sites, both Laughing Gulls and Forster’s Terns ducted in marshes where horses where present or ab- require Spartina for successful nesting, and they aggres- sent. The four most abundant species are shown. Error sively exclude other birds from nesting colonies (Bon- bars are 1 SE. The y-axis scales differ among some giorno 1970; Montevecchi 1978; Martin & Zwank 1987; graphs. Storey 1987). By consuming Spartina, horses destroy the nesting habitat of Laughing Gulls and Forster’s Terns, which ostensibly reduces the frequency of their aggres- dwelling in the mud. Xanthid crabs were thus the only sive interactions with other bird species. Consequently, predators capable of producing the difference in mum- horse-grazed marshes were characterized by a greater di- michog mortality we observed. versity of shore birds. The high densities of xanthid crabs that characterized horse-grazed marshes are prey for the many birds forag- Discussion ing in these marshes and may have contributed to the high numbers of foraging birds in these habitats (Table Our data suggest that grazing by horses indirectly pro- 1). Our results suggest, however that foraging by birds duces important changes in the communities of the salt was not the leading determinant of the size of xanthid marsh and adjacent subtidal waters. The removal of veg- crab populations, because both crab and crab-eating etation in the low marsh shifted the bird assemblage bird densities were highest in grazed marshes. Although from one dominated by colonial-nesting gulls and terns our study was not designed to address the processes af-

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Figure 3. (a) Proportion of tethered Fundulus hetero- clitus missing after 1 hour in 9-m2 plots in which Spar- tina alterniflora was removed or left intact. (b) Average proportion of fish missing from experimental plots with and without Spartina-like poles. In both (a) and (b) ***p 0.001. Figure 2. Mean number of fishes captured in minnow traps (n 15 per site) in horse-grazed and ungrazed marshes. Analyses were by analysis of variance: **p sults demonstrate that the presence of horses has effects 0.01; ***p 0.001. that are expressed throughout the marsh community, yet the elimination of horses from Shackleford Banks is legally forbidden. Conservation of the native marsh com- fecting xanthid crab populations, it appears that subtidal munity of Shackleford Banks will require resolution of predators (e.g., blue crabs [Callinectes sapidus] and the conflicting goals of maintaining feral horses and a fishes) may be more important to xanthid crab dynamics functioning marsh. than avian predators (Kneib 1982). Although large herbivores are generally absent from Our experimental enclosures isolated xanthid crabs as modern salt marshes, large, mammalian grazers were the only potential predator of our enclosed fish, and our common members of coastal communities during the results suggest that these crabs may be important fish Pleistocene. Carbon isotope values for Pleistocene herbi- predators (see also Kneib 1986). Thus, it appears that vores, including horses, bison, camels, and mammoths, when horses remove the shelter provided by Spartina, strongly suggest that these species foraged on Spartina mummichogs seek shelter in the burrows of xanthid when they occurred in salt marshes (Koch 1998; Koch crabs and then become easy prey for the crabs. We did et al. 1998). Consequently, Pleistocene marshes may not investigate the mechanisms by which grazing af- have functioned more like modern livestock-grazed fected pinfish abundance, although it is conceivable that marshes than like present-day marshes that lack large the same processes affecting mummichogs affect pin- herbivores. Our results suggest that the consumption of fish. It is significant that pinfish are transient, facultative Spartina biomass reduces the value of these marshes as residents of marshes and spend the majority of their nursery grounds for fishes and decapods. Fewer animals lives in seagrass meadows (Minello 1999). Thus, by af- moving between the marsh and associated habitats, in fecting pinfish using salt marshes, it is possible that concert with the high levels of herbivory, may also re- horses indirectly influence adjacent subtidal habitats. duce the export of productivity from the marsh surface, The suppression or removal of nonindigenous species potentially affecting the productivity of entire estuaries. in an effort to maintain natural communities is a key This scenario requires that interaction strengths between component of U.S. National Park Service (NPS) policy. Pleistocene grazers and Spartina were high enough to However, current legislation underlying the management produce indirect effects of the sort documented here of Shackleford Banks by the NPS (Shackleford Banks with feral horses. Densities of modern and Pleistocene Wild Horse Protection Act, Public Law 105–229) speci- large herbivores (Owen-Smith 1994) such as the feral fies a minimum of 100 horses and a target population horses on Shackleford Banks (Rubenstein 1981) were range of 100–110 animals. Further, the legislation speci- probably limited by food supply. Although predators fies that the natural resources on Shackleford Banks such as sabertooth cats were present in Pleistocene must not be “adversely impacted” by the horses. Our re- marshes (Koch 1998), available evidence suggests that

Conservation Biology Volume 16, No. 5, October 2002 1370 Effects of Feral Horses on Estuarine Habitat Levin et al. predation would have not functioned as a major limit on Davis, W. E. 1993. Black-crowned Night-Heron. No. 74 in A. Poole and the population size of large grazers (Owen-Smith 1994). F. Gill, editors. The birds of North America. The Academy of Natu- Modern large herbivores generally attain population ral Sciences of Philadelphia, Washington, D.C. Dijkema, K. S. 1990. Salt and brackish marshes around the Baltic Sea sizes close to the threshold for overexploitation of vege- and adjacent parts of the North Sea: their vegetation and manage- tation despite the presence of a diverse predator com- ment. Biological Conservation 51:191–209. munity (McNaughton 1993; Owen-Smith 1994). It is Dodd, S. L., and M. A. Colwell. 1998. 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