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(Reithrodontomys raviventris)

The salt marsh harvest mouse (Reithrodontomys raviventris; SMHM) is endemic to the San Francisco Bay Estuary, and is found generally only in the marshes surrounding the Bay (USFWS 2013).  The SMHM is small, about 10 grams, and probably lives less than a year in the wild, on average (Fisler 1965).  The species was listed as federally and state endangered by the U.S. Fish and Wildlife Service (USFWS) and the California Department of Fish and Wildlife in the early 1970’s due to habitat loss (USFWS 1984), as over 90% of the historic marshes in the San Francisco Estuary have been lost or altered (Goals Project 1999).  The SMHM diverged from its nearest common ancestor, the plains harvest mouse (R. montanus) about 4 million years ago (Bell et al. 2001; Statham et al. 2016).  By contrast, the tidal marshes of the San Francisco Estuary, as they exists today, only formed about 6,000 years ago (Goman et al. 2008).  This means that the SMHM has adapted to living in this landscape during only a very brief period in the species’ existence, and that the species did not evolve in or with the formation of the modern marshes, as researchers previously believed (Smith et al. 2018).  This is not to say that the species has no adaptations to life in tidal marshes, because it does, but it does mean that in the not too distant evolutionary part of the species, it utilized other habitat types, while today it is almost exclusively restricted to marsh habitats.  While there are still many unanswered research questions about SMHM, researchers over the past 5 decades have investigated many aspects of SMHM ecology (Smith et al. 2018).

There are two subspecies of SMHM.  Presumably, the northern subspecies is found in the marshes of Marin County on the West side of the central portion of the Bay, Contra Costa County on the East side, the marshes around San Pablo Bay extending north into Napa and Solano County, and Suisun Marsh and other marshes around Suisun and Grizzly Bays at the upper extent of the estuary.  The northern SMHM are characterized by having a long (>80.0 mm), thick (>2.0 mm) tail, much longer and thicker than the average western harvest mouse (R. megalotis; WHM) that occur sympatrically with SMHM (Statham et al. 2016).  The SMHM also tend to have much darker, richly colored fur with oranges, reds, and blacks dominant in the fur pattern.  The fur of WHM is most often drab grey-brown.  While the species name of SMHM, raviventris, means “red-bellied mouse,” individuals of the northern subspecies only rarely have fully red bellies, but commonly have small patches of red/orange on their throat and belly, which the WHM can also have, so this is not a good diagnostic character for identifying SMHM of the northern subspecies.  The SMHM tends to be docile, while WHM are often aggressive and frantic, and these differences in behavior are useful in differentiating the species.  The Southern SMHM presumably occurs in the marshes of Alameda County, and anywhere south of the Bay Bridge.  In these areas, the measurements of SMHM and WHM overlap substantially, and are not reliable for distinguishing between the species.  However, in the southern range, SMHM commonly occur with a full red/orange belly, which distinguishes them from WHM, along with other fur color and behavioral characteristics.  Still, in some cases, even the most experienced SMHM biologists rely on genetic sampling to accurately assign species identification to harvest mice in the San Francisco Estuary.  This is further complicated by the fact that biologists still do not have sufficient genetic data to confirm where the division between the two subspecies lies.

For decades, researchers believed that the SMHM was almost completely dependent on tidal marshes dominated by a pickleweed (Salicornia pacifica; USFWS 1984).  Over time, they found SMHM in other habitat types, such as diked and/or managed marshes, and marshes dominated by plants other than pickleweed such as alkali bulrush (Bolboschoenus maritima; Shellhammer et al. 2010).  Researchers also recorded SMHM moving into adjacent upland habitats during high tide events (Johnston 1957; Hadaway and Newman 1971). Recent research in the Suisun Marsh showed that populations of SMHM are equally large and healthy in tidal and managed marshes, and had not correlation with amount of pickleweed cover (Smith et al. 2019).  Over the years, captures of SMHM have been correlated with a variety of different plant cover types, heights, and structures (Zetterquist 1977; Gilroy and Shellhammer 1980; Shellhammer et al. 1982; Takekawa et al. 2001), but a taller, complex mix of plants with abundant pickleweed and fat hen (Atriplex prostrata) seems to be highly preferred by the SMHM (USFWS 2010).  Today, it is understood that the habitat use of SMHM is more flexible than biologists believed in the past, however, researchers are still trying to figure out what characteristics of various marsh habitats benefit SMHM the most, and why they seem to be restricted to that habitat type (Smith et al. 2018).  

 

When researchers still believed that SMHM were fully dependent on pickleweed for food and nesting habitat, it was easy to understand why SMHM are found almost exclusively in tidal marshes.  However, we now understand that the species eats a variety of different plants and invertebrates (Smith and Kelt 2019), and that population sizes can be equal in tidal and managed wetlands (Smith et al. 2019).  Further, recent telemetry work revealed that SMHM move throughout the microhabitats within the marsh ecosystem, and will readily cross levees, move into uplands, and swim across pools of water (Smith, Unpublished Data).  So the SMHM is capable of utilizing habitat types other than tidal marsh, and can eat a variety of foods, so why aren’t they found all over the place?  Researchers have recently started investigating the role of competition and predation in restricting SMHM to marsh habitats.  One older study indicated that when California voles (Microtus californicus)—which are much larger and more aggressive than SMHM—are abundant they push SMHM into the poorer quality habitat (Bias and Morrison 2006).  Also, the uplands adjacent to marsh habitats frequently are relatively open grasslands without substantial cover to hide from predators.  So it may be that, while SMHM would utilize upland habitats near marshes if they could, more aggressive rodents and predation pressure are forcing them to remain in the marshes, where environmental conditions can be a lot more unpredictable and challenging for a small rodent.  However, with the adaptations that SMHM have for life in marsh habitat, they are potentially the most competitive rodent in that ecosystem.

The SMHM is well adapted for life in its marsh environment.  Life in coastal marshes is stressful (Greenberg 2006).  Animals that live there must be able to survive without much fresh water, they may need to process very salty foods, they must be able to keep warm during cold wet winters since they can’t dig warm burrows on the saturated marsh plain, and they must be able to cope with, or escape from incoming tidal waters.  The SMHM is more highly adapted to cope with these stressors than other rodent species in the San Francisco Estuary (Fisler 1965).  

While the WHM, the upland associated cousin of the SMHM, is unable to survive on salty water, the SMHM is capable of surviving while drinking only water that is even saltier than sea water (Fisler 1963).  The SMHM is also capable of eating very salty marsh plants such as pickleweed and salt grass (Distichlis spicata).  While the physiological mechanism that the SMHM employs to cope with the large amount of salt in its diet has never been carefully investigated (because researchers generally can’t sacrifice individuals of an endangered species to study their internal physiology), at least one researcher attributed this ability to elevated kidney function (Fisler 1965).   

To cope with the environmental stressors of life in the marsh (cold moisture in the wet season, hot humidity in the dry season), the SMHM takes advantage of different aspects of its habitat.  While there is no evidence that the SMHM will dig burrows, it does use underground spaces when they are available (Trombley and Smith 2017).  Researchers observed SMHM utilizing existing burrows (presumably created by other rodents), crawdad burrows, deep cracks in dry mud, and the empty voids under decomposing plant hummocks (which are very cool and moist during the hot summer months).  They will also move up, taking over abandon wren and sparrow nests that are built in tall emergent vegetation, often over 4 feet above the ground (K. Smith, Unpublished Data).  A typical SMHM-built nest is about the size and shape of a chicken eggs, and are frequently nestled at the base of pickleweed plants, in salt grass, or in alkali heath (Frankenia salina).  These nests are loosely constructed, appearing to be relatively temporary.  This is not surprising considering the frequency of flooding in tidal marsh habitat.  SMHM presumably have no reason to expend significant energy constructing sturdy or elaborate nests when the next big high tide may wash it out to sea.  When those big tides do come, researchers have observed juvenile SMHM climbing up above nests into taller vegetation, while the nests is flooded.  Even at a young age, SMHM are capable of responding to and coping with the stress of tidal inundation.

Several times a year, however, there is even more extreme tidal flooding.  These very big high tides, associated with the periods when the moon is closest to and furthest from the earth, are called king tides.  In the winter, the king tides occur during the day, and in the summer they occur during the night.  During king tides, some marshes become completely inundated, and virtually all of the vegetation goes underwater.  In this case, even the strongest juveniles may not be able to escape the rising waters.  Adult SMHM presumably move into tall emergent vegetation or onto floating debris, if it exists, or into high elevation marsh or upland areas.  However, recent research has shown that during some king tides, there is not a mass exodus of SMHM into upland areas (K. Smith, unpublished data).  While biologist previously described these king tide periods as highly disturbing and dangerous for SMHM, with many individuals rushing to the upland edge where they are promptly consumed by hordes of predators lying in wait, recent research indicate this may not be the case.  The period of greatest inundation during any high tide lasts only dozens of minutes, and SMHM are capable of treading water for hours (Fisler 1965).  Further, trail cameras placed to detect terrestrial and aerial predators during king tides failed to identify substantially increased levels of predation during these periods (K. Smith, Unpublished Data).  While king tide periods are undoubtedly some of the most dangerous periods for SMHM, they may not be the highly traumatic events that biologists have envisioned for decades, and while some SMHM may drown (especially young still in nests), or be predated, it is likely that many survive these periods by swimming and clinging to tall vegetation or floating woody/plant debris, or occasionally moving into upland areas when they are within a reasonable distance.   

In past decades, researchers believed that SMHM primarily fed on, and thus were highly reliant on, pickleweed (USFWS 1984).  However, the SMHM has since been observed in areas with little to no pickleweed (Shellhammer et al. 2010; Sustaita et al. 2011; Smith et al. 2019).  A recent study documented SMHM eating more than 40 different species of plants and invertebrates (Smith and Kelt 2019).  Of the plants consumed, pickleweed was highly preferred, however, SMHM also spent substantial proportions of their time eating other species, especially non-native fat hen, rabbits-foot grass (Polypogon monspeliensis), and water grass (Echinochloa crus-galli).  And while Fisler reported that SMHM refused to consume insects when they were offered in a laboratory setting (1965), the recent diet preference study documented SMHM eating three different insect and crustacean species (e.g., beetles and amphipods).  While pickleweed undoubtedly composes a large proportion of the diet of SMHM where it is present, SMHM can and will eat a variety of native and non-native forbs, grasses (including nonnative annual grasses, and native grasses and bulrushes), and invertebrates (Smith and Kelt 2019).

The SMHM has historically been most threatened by habitat loss.  The vast majority of the tidal marshes that existed in the San Francisco Estuary and Sacramento-San Joaquin Delta before European colonization have been filled, diked, or otherwise modified or destroyed  (Goals Project 1999).  Marshes that remain are smaller, fragmented, and isolated (Takekawa et al. 2006).  These degraded marshes support smaller populations of SMHM that have little to no genetic connectivity.  Three notable exceptions are the Suisun Marsh, San Pablo Bay National Wildlife Area, and Don Edwards National Wildlife Refuge/Eden Landing Ecological Reserve.  In these areas, large tracts of habitat have been preserved or restored, and connectivity for SMHM is high.  However, they are still subject to threats other than historical habitat loss.

There are many modern threats to the already smaller and vulnerable patches of tidal marsh habitat and populations of SMHM that remain in the San Francisco Estuary including invasive plant and animals species, chronic environmental contaminants, the risk of petroleum or other chemical spills, and climate change (Smith et al. 2018).  Invasive predators like feral cats (Felis catus) and competitors like house mice (Mus musculus) can impact SMHM directly though processes such as predation, aggression, and disease/parasite transmission, or indirectly via processes like stress and resource depletion.  Invasive plants like smooth cordgrass (Spartina alterniflora), common reed (Phragmites australis), and perennial pepperweed (Lepidium latifolium) can alter habitat structure and may displace native flora and fauna (Takekawa et al. 2006; Estrella and Kneitel 2011; Wigginton et al. 2014). The threat of environmental contamination such as heavy metals, organochlorines, PCBs, or oil spills on SMHM is understudied, even though virtually all SMHM habitat is bordered by dense urban and suburban development, and busy maritime shipping routes where petroleum products, pesticides, and detergents are constantly entering their semi-aquatic habitat.  The only study to examine this issue found that SMHM were absent from all areas where house mouse livers contained elevated mercury and PCB concentrations (Clark et al. 1992). The SMHM is also at risk from catastrophic chemical disturbance, such as oil spills from refineries, pipelines, or ships.  

In addition to the above threats, SMHM is at ongoing and increasing threat from climate change and associated sea level rise (USFWS 2010; Thorne et al. 2012).  Research projects a net loss of SMHM habitat as some areas of mid- and high-marsh become low- or mid-marsh, and some low-marsh converts to mud flat, especially where marshes lack area to migrate upland, and either time or sediment input for accretion in response to rising sea level (Takekawa et al. 2006; Thorne et al. 2012).  The more recent analyses project sea-level rise to exceed 1.66-2 meters (Oppenheimer and Alley 2016), indicating that losses may be much more severe than previously estimated (Thorne et al. 2018).  Other effects of climate change like increased temperatures, reduced snowpack, more frequent and extreme weather events (prolonged drought, extreme storms, and king tides) will compound the harmful effects of sea-level rise effects and saltwater intrusion in the estuary (Dettinger et al. 2016).

Toggle ContentThe SMHM has been addressed in two separate USFWS federal recovery plans, the Salt Marsh Harvest Mouse and California Clapper Rail Recovery Plan (USFWS 1984) and the Recovery Plan for Tidal Marsh Ecosystems of Northern and Central California (USFWS 2013).  These plans outline threats to the species, actions that should be taken to help the species rebound, and criteria that must be met for the species to be down-listed from Endangered to Threatened, or de-listed completely.

The original recovery plan, which addressed only the SMHM and California Ridgway’s rail (formerly California clapper rail) recommended protecting large existing marshes, restoring diked marshes to tidal action, restoring upland transition zones, performing research on human activities that could impact habitat, performing research on marsh accretion and erosion dynamics, and to perform habitat management (USFWS 1984).  The updated recovery plan, which addresses the entire ecosystem, recommended protecting, restoring, managing and monitoring existing tidal wetlands, conducting range-wide SMHM monitoring, conduct research as necessary such as demographic analyses and habitat restoration and management techniques, and to improve coordination and participation by researchers and managers, and increased public outreach efforts.  For down-listing to threatened, the 1984 recovery plan required acquisition and management of 3,900 hectares of occupied, public agency-owned essential habitat, and either 3,200 hectares of occupied, privately owned essential habitat, or 7,000 hectares of tidal and diked baylands.  Full delisting required an additional 3,000 hectares of essential habitat and restoration on wildlife refuges within the species range.

For down-listing the updated recovery plan, finalized in 2013, broke down the required acreage of protected habitat (totaling 6,100 hectares) by bay, with ~2,500 in the Central and South San Francisco Bay, ~1,800 in San Pablo Bay, and ~1,800 in Suisun Bay.  It also required 3-5% catch per unit effort during annual SMHM population surveys in designated areas, and reduction and control of invasive plants. For full delisting, this plan also required implementation of the Suisun Marsh Habitat Management, Preservation, and Restoration Plan, the South Bay Salt Pond Restoration Plan, and the development of an oil spill response plan, in addition to the creation and preservation of high marsh and upland habitat to accommodate sea level rise.  

Currently, management for SMHM differs among land-owners and agencies.  Especially in the South San Francisco Bay, acquisition of non-tidal lands—especially old salt production ponds—for restoration to tidal action is a priority, and has results in the conversion of thousands of hectares of previously unsuitable land to potential SMHM habitat within the past several decades.  In the northern SMHM range, substantial amounts of non-tidal, diked wetlands, which already support SMHM exist.  In one such area, the Suisun Marsh, populations of SMHM in diked and managed wetlands equal those in tidal wetlands, and conversion of these areas to tidal action may have little to no value for local SMHM populations (Smith et al. 2019), so protection and enhancement of diked wetlands is a priority, in addition to tidal restoration.  In some cases, restoration of diked wetlands to tidal action will result in a reduction in acreage of SMHM habitat, as some areas become permanently subtidal.  Therefore, habitat restoration and enhancement actions must take into account both local conditions, as well as existing populations of SMHM at potential sites.

Accretion – the process of growth or increase, typically by the gradual accumulation of additional layers or matter.

Adaptation – a change or the process of change by which an organism or species becomes better suited to its environment.

Endangered Species – a species that is very likely to become extinct in the near future, either worldwide or in a particular political jurisdiction.

Endemic – native and found only in a certain area.

Erosion – the action of surface processes (such as water flow or wind) that removes soil, rock, or dissolved material from an area.

Extinct – no longer in existence; having ended or died out.

Physiological – relating to the way in which a living organism or bodily part functions.

Species – a group of living organisms consisting of similar individuals capable of exchanging genes or interbreeding. 

Sympatric – animals or plants, especially of related species or populations, occurring within the same geographical area; overlapping in distribution.

Threatened Species – any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range. 

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